Accepted Manuscript Title: Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice Author: P. Azizi, M.Y. Rafii, M. Maziah, S.N.A. Abdullah, M.M. Hanafi, M.A. Latif, A.A. Rashid, M. Sahebi PII: DOI: Reference:
S0925-4773(14)00068-9 http://dx.doi.org/doi: 10.1016/j.mod.2014.11.001 MOD 3317
To appear in:
Mechanisms of Development
Received date: Revised date: Accepted date:
15-4-2014 5-11-2014 14-11-2014
Please cite this article as: P. Azizi, M.Y. Rafii, M. Maziah, S.N.A. Abdullah, M.M. Hanafi, M.A. Latif, A.A. Rashid, M. Sahebi, Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice, Mechanisms of Development (2014), http://dx.doi.org/doi: 10.1016/j.mod.2014.11.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice P. Azizi1, M.Y. Rafii1, M. Maziah2, S. N. A. Abdullah3, M.M. Hanafi1, M.A. Latif1, A.A. Rashid4, M. Sahebi1
1
Laboratory of Food Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400
Serdang,Selangor, Malaysia. 2
Department of Biochemistry, Faculty of Biotechnology and BiomolecularScience, Universiti Putra
Malaysia, 43400 Serdang,Selangor, Malaysia. 3
Laboratory of Crop Science, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400 Serdang,
Selangor, Malaysia. 4
Department of Agriculture Technology, Faculty of Agriculture, Universiti Putra Malaysia, 43400
Serdang,Selangor, Malaysia.
Corresponding author: M.Y. Rafii [email protected] .
Highlights
Cytokinin has been elucidated as a promoter of branching, resulting in increased spikelet numbers in rice.
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Auxin provided by the primary shoot apex suppresses axillary bud growth; however, CK reduces the inhibition and leads to the outgrowth of lateral branches.
The decreased level of CK resulted in the increasing of apical dominance and represses the growth of axillary bud.
Graphical Abstract
Abstract
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Auxin and cytokinin regulate different critical processes involved in plant growth and environmental feedbacks. These plant hormones act either synergistically or antagonistically to control the organisation, formation and maintenance of meristem. Meristem cells can be divided to generate new tissues and organs at the locations of plant postembryonic development. The aboveground plant organs are created by the shoot apical meristem (SAM). It has been proposed that the phytohormone, cytokinin, plays a positive role in the shoot meristem function, promotes cell expansion and promotes an increasing size of the meristem in Arabidopsis, whereas it has the reverse effects in the root apical meristem (RAM). Over the last few decades, it has been believed that the apically derived auxin suppresses the shoot branching by inactivating the axillary buds.However, it has recently become clear that the mechanism of action of auxinis indirect and multifaceted. In higher plants, the regulatory mechanisms of the SAM formation and organ separation are mostly unknown. This study reviews the effects and functions of cytokinin and auxin at the shoot apical meristem. This study also highlights the merger of the transcription factor activity with the actions of cytokinin/auxin and their complex interactions with the shoot meristem in rice.
Keywords: Stem cells, Transcription factors, cell expansion, axillary buds.
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Contents Abstract ................................................................................................................................. 1 1 Introduction ................................................................................................................... 4 2 Hormonal Pathways required for SAM maintenance and functions ............................ 6 2.1
Cytokinin actions on the SAM ............................................................................... 6
2.1.1 2.2
Cytokinin signaling transduction in rice ......................................................... 8
Auxin signaling in the SAM................................. Error! Bookmark not defined.
2.2.1 2.2.2
Auxin and the shoot branching pattern (Tillering) in rice ............................ 14 Auxin and Panicle formation in rice ............. Error! Bookmark not defined.
3 4 5 6
Auxin/Cytokinin crosstalk and other hormones in SAM ............................................ 16 Conclusion .................................................................................................................. 19 Acknowledgements ..................................................................................................... 19 References ................................................................... Error! Bookmark not defined.
1
Introduction
The stem cells of plant meristems play different roles in the growth and development of new organs over the plant lifetime. All of the post-embryonically shaped organs and tissues are produced from pluripotent stem cells that exist in the growing tips of the plants, namely the shoot apical meristem (SAM) and the root apical meristem (RAM). The aboveground organs in plants are created by the SAM, whereas the belowground organs are formed through the RAM. In monocotyledons, most of the plant parts are generated from the SAM because the root system consists primarily of adventitious roots, with a small portion consisting of radicle. The mechanisms of SAM development during embryogenesis and maintenance and its roles in the postembryonic growth are the primary concern in plant developmental biology. Stem cells in the SAM are constantly selfrenewing, instinctive and can develop into all of the types of cells that form the shoot components (Itoh et al., 2000). For example, the leaf is the essential lateral organ and is repetitively derived from the SAM. The final leaf shape, the plastochron and the phyllotaxy are organised by the SAM in rice (Kawakatsu et al., 2009 and Heisler et al., 2005). Generally, the procedure of SAM formation during embryogenesis is divided in three phases. The first phase determines the axes during the beginning stage of embryogenesis. The next phase generates and senses regional information to locate the SAM inside of the embryo. The final phase is the SAM formation. Embryogenesis in monocots differs from that in other plants, such as Arabidopsis (Reviewd in Itoh et al., 2005), regarding several specific
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features. For example, several organs are specifically produced in rice involving the scutellum, epiblast and coleoptiles. Moreover, in the early stage of embryogenesis until the end of the globular steps, the rice embryo does not follow a stereotypical pattern of cell division, and the division directions are not fixed. In contrast, other cells have shown a stereotypical division pattern during the early stages of embryogenesis. In Arabidopsis, the cell lineage-related information may affect the specific location of SAM and other organs in the post-embryogenesis stages (Capron et al., 2009). However, because of the non-conserved cell divisions pattern, rice cells must detect their locations, which are created by externally or internally positional information independent of the cell lineage in the early stages of embryogenesis. In monocots, the SAM is formed laterally at the base of their single cotyledon. During the post-embryonic stages, various organs, including leaves, stems and axillary buds, are generated by the SAM while the indistinctive stem cell populations are maintained. The SAM of most of the angiosperms is planned into a central zone, containing gradually and continually dividing stem cells, and a peripheral zone, composed of the cells with the ability to rapidly divide and that can be integrated into the organ primordial (Reviewed in Zadnikova and Simon, 2014 and Kerstetter and Hake, 1997). The central region of the SAM in cereal crops is surrounded by two different dividing cell layers (L1 and L2), which tend to be taller and finger shaped. This region of the SAM includes three layers (L1, L2, and L3) in dicots (Reviewed in Sticklen and Oraby, 2005 and Steeves and Sussex, 1989). To date, different detailed aspects of the apical meristem have been considered. Auxin and cytokinin, as two plant growth regulators, play relatively essential roles in many features of plant development. Furthermore, the interaction between auxin and cytokinin is important for the regulation of a few developmental processes, such as the formation and maintenance of the meristem, which are crucial mechanisms for the establishment of the intact plant (Reviewed in Zhao, 2008, Ashikari et al., 2005, Giulini et al., 2004, Reinhardt et al., 2003 and Reinhardt et al., 2000). Cytokinin positively modulates cell division and proliferation in the shoot stem cell regions; in addition, the organising centre in the central region is a highly cytokinin sensitive area of the SAM (Reviewed in Murray et al., 2012, Riou-Khamlichi et al., 1999 and Skoog and Miller, 1957). The root and SAM patterning and lateral organ development are also regulated by auxin in the postembryonal development stages (Benkova et al., 2003). The importance of SAM inspires an increased focus on the effective mechanisms involved in its function and maintenance. In this study, we review the molecular mechanisms of cytokinin and auxin at the shoot apical meristem and highlight the merger of the transcription factor activity with the actions of cytokinin and auxin and their complex interactions with the shoot meristem in rice.
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2
Hormonal Pathways required for SAM maintenance and functions
Physiological studies have revealed the vital role of two phytohormones, cytokinins (CKs) and auxins, in the control of axillary bud growth. Generally, auxin is produced by the primary shoot apex cells, which inhibit the development of axillary buds; however, this inhibition is relieved by CK to enable the development of the lateral branches (Tanaka et al., 2006). Therefore, the growth of the axillary buds is controlled positively and negatively via the CKs and auxins, respectively.
2.1
Cytokinin actions on the SAM
Cytokinin plays roles in various aspects of plant growth, including leaf senescence, apical dominances, shoot meristem activity and formation, nutrient mobilisation, seed germination, and the response to stresses (Riefler et al., 2006, Werner et al., 2003 and Srivastava, 2002). Moreover, CK directly affects the lateral root founder cells to suppress the root initiation (Laplaze et al., 2007). The regulation of the CK activity is similar to other plant hormones in which the maintenance of the balance among its synthesis, degradation, inactivation, reactivation, and so on is required (Reviewed in Sakakibara, 2006). N6Isopentenyladenine (iP) and trans-Zeatin (tZ), which are common natural isoprenoid CKs, are originally the products of the methylerythritol phosphate (MEP) pathway, whereas a large portion of cis-Zeatin (Cz) is obtained from the mevalonate (MVA) pathway. ATP, ADP and AMP are converted to the iPRT, iPRDP, and iPRMP forms, respectively, by adenosine phosphate-isopentenyl-transferase (IPT). IPTs are encoded by a small gene family that includes at least eight members in rice plants (OsIPT1 to OsIPT8) (Sakamoto et al., 2006). Among these transcriptional factors, the expression of theOsIPT2 and OsIPT3 genes is induced by OSH1. The nucleotides entering the CK pathway are converted to tZ-nucleotides by CYP735A, whereas iP, tZ, dZ and cZ can be catabolised by the expression of the LONELY GUY (LOG) gene or by a function of adenosine nucleosidase in this pathway (Fig. 2) (Kurakawa et al., 2007 and Sakamoto et al., 2006). The LOG gene is expressed in the apical zone of the rice meristem tissue, which contains stem cells. Loss of function mutations in the LOG locus have been shown to reduce the meristemal cell number, and ultimately reduce the SAM size (Kurakawa et al., 2007); consequently, these plants formed small panicles with imperfect flowers. In maize, theKnotted-1 (Kn1) mutants have shown a smaller meristem size compared with the normal plants (Vollbrecht et al., 2000). The orthologs of kn1, STM in Arabidopsis (Long et al., 1996)and OSH1 inrice (Tsuda et al., 2011) have also displayed meristem termination phenotypes.
In recent studies, the discovery of the mechanistic links between the
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transcription systems controlling the SAM activity and the hormone biosynthesis and signalling has been reported (Jasinski et al., 2005, Leibfried et al., 2005, Hay et al., 2002 and Sakamoto et al., 2001). Furthermore, CKs are negative regulators of the root meristem activity, which opposes their promotional role in the shoot organogenesis. The encouraging role of CK on the SAM activity has been confirmed by a mutation analysis of the cytokinin receptor genes in plant species (Higuchi et al., 2004 and Nishimura et al., 2004). These processes occurred by the downstream components of the CKsignalling pathway after its perception and signal transduction (Fig. 1). The effects of these components are not always directly through CK but also by interactions with other hormones or transcription factor complexes (Reviewed in Gupta and Rashotte, 2012). Cytokinin also mediates a number of lightregulated processes, including chloroplast differentiation and de-etiolation (Nemhauser and Chory, 2002); in addition, certain CK functions are primarily executed through the control of the cell cycle activities (Roef and Van Onckelen, 2010). The number of cell divisions and exiting cells from the proliferation state in the meristem basal border are regulated by CK. Exogenous CK primarily decreases the elongation of the wild-type roots by reducing the cell expansion and the size of the meristem rather than by dropping the cell division rate (Werner et al., 2003 and Beemster and Baskin, 2000). It has also been reported that transcriptional factors, such as KNOTTED-like homeo box (KNOX), are dependent on the biosynthesis of CK in meristem cells; in addition, an analysis of the KNOX mutants of rice has shown that the expression of the KNOX gene is positively regulated by the action of CK and KNOX genes themselves (Tsuda et al., 2011). The KNOX proteins, which are encoded by the KNOX genes, have been shown to accumulate in the cells around the SAM. This transcription factor is required for the maintenance of SAM and its activity (Sakamoto et al., 2006, Jasinski et al., 2005 and Yanai et al., 2005). It has also been revealed that OSH1 directly attaches to the five KNOX loci in the rice genome, whichincludesOSH1 and OSH15, by the conserved cis-elements. The positive auto-regulation of OSH1 is an essential factor for its expression and the SAM maintenance.
Thus, the preservation of the
indistinctive state mediated by the positive auto-regulation of a KNOX gene is a requisite mechanism of self-maintenance of the SAM (Tsuda et al., 2011). It has been defined that KNOX 1binds to thousands of loci in the maize genome containing 643 genes that are adapted in one or several tissues. KNOX 1 also binds to the cis-elements present in the high confidence KNOX1-bound loci in the maize. KNOX 1 directly regulates the genes participating in hormonal pathways, especially auxin and TFs with the home box (HB), which affects the plant meristem characteristics and function (Bolduc et al., 2012). Several classes of transcription factors have been shown to participate in the SAM development (Table 1) (Kurakawa et al., 2007 and Leibfried et al., 2005). One of the most important traits in rice is the grain
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yield per panicle, which is controlled by the DENSE AND ERECT PANICLE1 (DEP1) (Huang et al., 2009), the WEALTHYFARMER’S PANICLE (WFP), Gn1a (Ashikari et al., 2005), ect QTL loci. Among these genes, Gn1a encodes a cytokinin degradation enzyme (OsCKX2). There is a negative correlation between the expression level of OsCKX2 and the grain yield per plant, confirming the positive influence of the CKs on the grain number per plant. A decreased expression of OsCKX2 leads to CK accumulation within the inflorescence meristems and raises the quantity of the reproductive organs, causing an improved grain yield (Ashikari et al., 2005).
2.1.1 Cytokinin signalling transduction in rice Plants use the two-component phosphorelay systems for signal transduction and the aspects of these two-component systems (TCS), which have been suggested in plant responses to the Cytokinin (Reviewed in Hwang et al., 2002 and Schaller, 2000). A simple TCS is composed of a His sensor kinase (HK) and a response regulator (RR). The His kinase autophosphorylates the conserved His remains in response to the environmental stimulus. This particular phosphate group can then be transferred to the conserved Asp remains inside of the receiver domain of the response regulator.
This response
regulator, which is typically a transcription factor, subsequently regulates the downstream signalling in the pathway. Multistep phosphorelay systems are also identified, which use three elements: a hybrid receptor kinase containing the His kinase and receiver domains in a single protein, a phosphotransfer protein that contains His (HPt), and a response regulator (Schaller, 2000 and Reviewed in Swanson et al., 1994). In the multiple phosphorelay, the particular phosphate is transmitted from amino acid to amino acid between proteins in the sequence His-Asp-His-Asp. In Arabidopsis, the RRs are categorised into type-A (primary CK response genes), -B and -C classes, depending on their amino acid sequences and their domain structure (Reviewed in Lomin et al., 2012, Sakai et al., 2001, Sakai et al., 2000, Kiba et al., 1999, Brandstatter and Kieber, 1998, Sakai et al., 1998 and Taniguchi et al., 1998). The type-A ARRs consist of a receptor domain with a short sequence extension at the N- and the C-terminal ends (Ramireddy, 2009). Variable transcription levels of certain type-A ARRs under biotic and abiotic stresses have been reported (Jeon and Kim, 2013, Jeon et al., 2010, Mason et al., 2010, Wohlbach et al., 2008 and Hass et al., 2004). The GARP (or B motif) domain binding sites are located in the promoters of the type-A ARRs. The GARP is B motif homologous in the type-B ARRs, which generally occur in the GARP family of plant transcription factors (Hosoda et al., 2002). The type-B ARRs may bind to these promoters
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and operate the transcription (Sakai et al., 2000). As opposed to the type-A ARRs, the expression level of the type-B ARRs is unaffected by CKs, nitrate, or other plant hormones (Hirose et al., 2007, Imamura et al., 1999 and Lohrmann et al., 1999). Several studies have shown that the type-C ARR genes cannot also be activated by CK (Gattolin et al., 2006). Others studies have mentioned that the type-C ARRs may play different roles in the CK-signalling pathway (Horak et al., 2008). The transcription levels of most of the OsRRs genes are quickly enhanced under exogenous CK application in rice (Du et al., 2007). However, the type-B ARRs include a receptor domain and a large C-terminal. In Arabidopsis, three Hissensor kinases involving Arabidopsis Histidine Kinase 2 (AHK2), AHK3 and AHK4 are cytokinin receptors (Inoue et al., 2001, Suzuki et al., 2001, Ueguchi et al., 2001 and Yamada et al., 2001). These CK receivers (AHK2, AHK3 and AHK4) are effective in the shoot and root development, leaf senescence, seed size, germination, and the metabolism of CKs in Arabidopsis and maize (Wang et al., 2014, Reviewed in ElShowk et al., 2013 and Riefler et al., 2006). AHK4 is known as Cytokinin Response 1 (CRE1) or Wooden Leg 1 (WOL1), which is a primary receptor directly bound to a variety of CKs (natural and synthetic) in a significantly specific manner in Arabidopsis. A single amino acid replacement (Thr-301 to Ile) in the extracellular domain of AHK4 results in its incapability to bind to the CKs. This mutation confirmed the transducer role of AHK4 and its two homologues, AHK2 and AHK3, for the CK signals across the plasma membrane (PM) in Arabidopsis. The His-kinase activity of AHK4 is promoted by the direct attachment of CK to the extracellular domain. Thus, AHK4alone distributes these hormonal signals through the membrane (Yamada et al., 2001). Subsequently, the signals are transmitted by the HPs to the RRs in the nucleus, which suppress or activate transcription. Two additional His sensor kinases, Cytokinin Insensitive 1 (CKI1) and AHK1, include a putative ligand binding domain that does not have a significant similarity to the ligand domains of the cytokinin receptors, indicating their particular involvement in the sensing of additional stimuli (Schaller et al., 2008). The TCS pathways are have clearly been suggested as a factor in the plant’s response to cytokinin, which is considered to incorporate all of the components of a multistep phosphorelay system (Hwang and Sheen, 2001). Based on the recommended model, the CK receptors autophosphorylate in response to CK. This phosphate can then be transmitted to an HPt protein, which then travels into the nucleus and triggers the type-B ARRs by transporting the phosphate to them. One of several transcriptional targets of the type-B ARRs is typically the type-A ARRs that upon induction, act as negative modulators of the primary signal transduction pathway (To et al., 2004). To date, the most powerful proof for the function of the type-B ARRs in regulating the CK signal has been derived from the
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analysis of ARR1. A null mutation within ARR1 leads to a diminished sensitivity to CK in shoot regeneration and root elongation assays (Sakai et al., 2001). In Arabidopsis, over-expression of ARR1 and ARR2 causes an increased sensitivity to CK (Hwang and Sheen, 2001 and Sakai et al., 2001). There are ten type-A ARRs, which arrange into five similar pairs. The actual transcription rates of most of the type-A ARRs (not the type-B ARRs) are typically quickly and particularly activated in response to the exogenous CK, and this activation occurs in the absence of de novo protein synthesis (D'Agostino et al., 2000 and Taniguchi et al., 1998). The gene expression differs among the various type-A ARRs, with ARR4, ARR8, and ARR9 showing relatively high basal ranges, and ARR5, ARR6, ARR7 and ARR15 displaying the maximum fold induction in response to CK (Rashotte et al., 2003 and D'Agostino et al., 2000). The transcription of the type-A ARRs is regulated simply by the type-B ARRs (Hwang and Sheen, 2001 and Sakai et al., 2001). Over-expression of several type-A ARRs suppresses the expression of the ARR6 promoter-luciferase reporter in the cell culture of Arabidopsis, indicating that the type-A ARRs can adversely regulate their particular transcription (Hwang and Sheen, 2001). The homologs of the type-A ARRs and type-B ARRs are found in various other dicotyledonous and monocotyledonous plants, such as maize (Zea mays L.) and rice (Oryza sativa L.) (Asakura et al., 2003 and Reviewed in Haberer and Kieber, 2002). In rice, two CK-signalling pathways have been suggested; one pathway is mediated by the twocomponent regulatory systems, and the other pathway is mediated using CHARK (CHASE domain Receptor-like serine/threonine Kinase) through serine/threonine phosphorylation (Tsai et al., 2012, Yonekura-Sakakibara et al., 2004 and Reviewed in Hutchison and Kieber, 2002). The CK signalling system in rice, which is the same as that in Arabidopsis, typically includes a sensory histidine kinase (HK), a histidine phosphotransfer protein (HP) and a response regulator (RR) (Fig. 1); however, whether the roles of the rice HPs have diverged remains unclear. In rice plants, five different CK-response histidine protein kinases (HKs) (OsHK1-4, and OsHKL1), fifteen response regulators (type-A OsRRs) (OsRR1-15), seven type-B OsRR genes (OsRR16-22), five pseudo-response regulators (OsPRR1-5) and two Authentic HPs (OsAHP1 and OsAHP2) have been identified (Sun et al., 2014 and Du et al., 2007). The Ehd1, a typeB OsRR with a novel two-component signalling cascade, is integrated in the photoperiodic control pathway of flowering in rice (Du et al., 2007). The OsAHPs phosphorylate the type-A and type-B OsRRs in the nucleus of rice cells. The phosphorylated type-A OsRRs can initiate transcription of the target genes (CYTOKININ RESPONSE FACTOR (CRF) and type-A OsRRs genes). The type-A OsRRs, as negative inhibitors of the CK signalling, receive phosphoryl groups from the OsAHPs. The type-A OsRRs are stabilised by phosphorylation; otherwise, its protein will be degraded. The CRFs mediate the CK
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responses accompanied by the His-Asp phosphorelay system (Rashotte et al., 2006) and promote the transcription of the CK response genes. Several targets of the CRFs and the type-B OsRRs are collective, although certain targets are specific to the each of them. In these schemes, the signals are transferred through the phosphoryl groups bound to the histidine and aspartic residues. Membrane-located HK plays a role as a sensor of the CKs. In the second CK-signalling pathway, the transporter domain individually includes a typical sequence motif and a histidine residue and is the location of the auto phosphorylation (Reviewed in West and Stock, 2001). A domain, which is a putative recognition site for CK shared by all of the HKs, was identified during the prediction of the extracytoplasmic regions and the design of cyclase/histidine kinase-associated sensory extracellular (CHASE) domains (Anantharaman and Aravind, 2001, Ueguchi et al., 2001 and Yamada et al., 2001). The CHASE domain is located outside of the PM and binds CK. Binding of CK motivates conformational changes in the proteins, which activate the transfer of a phosphoryl group between the conserved phosphor-admitting His and Asp residues. The OsAHPs (Authentic HPs) are transported through the nuclear membrane (NM) to the nucleus when they are phosphorylated in rice (Sun et al., 2014). AtHK1, a putative osmosensor, has been identified to interact with AtHPt1 (a phosphotransfer protein) in Arabidopsis. A similar interaction has been found between OsHK3b, the ortholog of AtHK1, and OsHPt2 in rice. The presence of a transmitter domain (TD) and a receiver domain (RD) has been confirmed in AtHK1 by analysis of its amino acid sequence, whereasOsHK3b contains three conserved domains known as CHASE, TD and RD. A binding analysis of the RD domain of these sensors in Arabidopsis and rice has confirmed the role of the different residues, such as His in the HPt protein, which is required for their interaction (Kushwaha et al., 2014).
2.1
Auxin signalling in the SAM
Auxins, as with other phytohormones, can control many aspects of plant growth and development. These features are involved in the branching of the shoot and root and in the differentiation of the vascular system (Reviewed in Leyser, 2006 and Reinhardt et al., 2000). Over the past decade, it has been shown that auxin plays roles not only as the primary regulator of organogenesis at the SAM but also as a central determinant of the self-organising characteristics of phyllotaxis (Reviewed in Sassi and Vernoux, 2013 and Reinhardt et al., 2003). Five tryptophan (TRP) auxin biosynthetic pathways have been reported. Four of these pathways are TRP-dependent, including the indole-3-pyruvic acid (IPA), indole-3-acetaldoxime (IAOx), tryptamine (TAM), and indole-3-acetamide (IAM) pathways, and one pathway is TRP-independent in monocots, such as rice (Fig. 3). The IAM is converted to IAA through the action of the amidase genes. These genes have not yet been characterised in monocots, although an
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IAM hydrolase activity has been identified in rice callus; therefore, it appears that this pathway is used in grasses (Arai et al., 2004). The IPA pathway is important in the monocot and dicot growth. TRPaminotransferase genes, such as TAR1 and TAA1, convert TRP to IPA in Arabidopsis (Stepanova et al., 2008 and Tao et al., 2008). TAA1-like genes have not yet been identified in rice. It has been suggested that IPA is changed to indole-3-acetaldehyde (IAAId) through the IPA decarboxylase activity; furthermore, IAAId is converted to IAA by an aldehyde oxidase, which is encoded by the OsAO1 gene in rice (Yamamoto et al., 2007). The TAM pathway plays an important role in different developmental stages of monocots and dicots. The auxin biosynthesis is regulated by several gene families. The YUC gene family is involved in auxin biosynthesis and encodes flavin mono oxygenase-like enzymes that are responsible for regulating the TAM pathway.
YUC can convert tryptamine (TAM) to N-
hydroxytryptamine (NHT) in vitro, suggesting that the N-oxygenation of TAM, a rate limiting step in the biosynthesis of auxin in plants, is catalysed by YUC. Among the 13 YUC-like genes identified in rice, only two (OsYUCCA1 and CONSTITUTIVELY WILTED1 (OsCOW1)) have been functionally studied (Woo et al., 2007 and Yamamoto et al., 2007). Over-expression of OsYUCCA1 has shown enhanced IAA levels and has been attributed to the over-production of the auxin phenotypes, whereas plants expressing the antisense OsYUCCA1 cDNA have shown problems that resemble those of the rice auxin-insensitive mutants. These findings have demonstrated the crucial role for the OsYUCCA1 in the IAA biosynthesis through the TRP-dependent pathway. In addition, homozygous plants with the inserted OsCOW1 gene, which encodes a member of the YUCCA family of proteins, have shown decreased leaf widths and root to shoot ratios. Once the oscow1 seedlings have been grown under low intensity light and increased relative humidity, the rolled leaf characteristic is significantly improved. Therefore, these observations have suggested that OsCOW1- mediated IAA biosynthesis has an important role in conserving the root to shoot ratios, thus affecting water homeostasis in rice.
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After the identification of this family, it was demonstrated that this gene family maintains excellent control of the auxin biosynthesis and plays a basic role in the shoot meristem activity (Zhao et al., 2001). The IAOx pathway is believed to be active only in cruciferous species, such as Arabidopsis, but there is contradictory evidence suggesting that this pathway may also occur in monocots (Sugawara et al., 2009). For example, indole-3-acetonitrile (IAN) is converted to IAA by the action of the nitrilase genes in Arabidopsis.
Nitrilase genes have also been identified in maize (ZmNIT2) (Park et al., 2003).
Additionally, genes analogous to ZmNIT2 have been reported but not characterised in rice (Yamamoto et al., 2007). Organ pericarp mutants in maize have also been studied; the mutants show an inability to produce TRP but continued to produce auxin. It has been confirmed that TRP-independent biosynthesis occurs in maize (Wright et al., 1991). When auxin is not produced from TRP, it is thought to be made through indole-3-glycerol phosphate or indole; however, the genes involved in this pathway have not been characterised for monocots or dicots (Reviewed in Woodward and Bartel, 2005). It has been demonstrated that auxin moves between cells along the shoot-root axis in a polar manner with the help of carrier proteins involving influx and efflux carriers (Sieberer and Leyser, 2006) (Table 2), although the regulation and differentiation of the tissue in response to auxin varies locally (Kramer and Bennett, 2006, Weijers et al., 2005, Benkova et al., 2003 and Reinhardt et al., 2003). Moreover, the concentrations of the local auxin are under the control of an active combination of polar auxin transport, auxin synthesis, catabolism, and conjugation in the shoot meristem cells. A gene family of 31 members produces the Auxin/IAA proteins in rice (Jain et al., 2006). These proteins are short-lived transcriptional regulators that mediate theauxin responses accompanied by the F-box protein transport inhibitor response1 (TIR1) protein, an auxin receptor. The OsIAA1/3gene was the first reported AUX/IAA gene in rice. Auxin induces the transcription of OsIAA1/3; however, light suppresses its expression (Nakamura et al., 2006, Thakur et al., 2001). Alternatively, OsIAA1/3 is expressed in nearly all of the plant organs and tissues (Song et al., 2009). OsIAA4 encodes a protein that contains 204 amino acids with four domains. OsIAA4 has the same domain II as AtIAA31, containing a G-to-D substitution. In Arabidopsis, shy2-3, iaa18-1 and AtAA31 include a dominant mutation-type domain II that would result in a dominant mutation of the Aux/IAA genes. Its core amino acid motif is “DWPPV/I”, although the canonical Aux/IAA protein contains a core motif of domain II known as “GWPPV”; therefore, OsIAA4 can
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be considered as a dominant-mutation class of protein in rice. The over-expression of the OsIAA4 gene in rice plants has illustrated dwarfism, enhanced tiller angles, decreased gravity response and less sensitivity to 2,4-dichlorophenoxyacetic acid (2,4-D) (Song and Xu, 2013).
2.1.1 Auxin and the shoot branching pattern (Tillering) in rice A shoot branching pattern is an important factor in plant architecture. This pattern is arranged by the following two independent stages: the formation of axillary lateral buds in the axil of the leaves followed by bud outgrowth. The apical dominance, as a central mechanism, suppresses the axillary bud growth through the apical meristem growth (McSteen and Leyser, 2005). The presence of the SAM affects the suppression of the lateral bud outgrowth, whereas the lateral bud is initiated by the removal of this meristem (Beveridge, 2006). The apically derived auxin suppresses the bud activity, whereas CK promotes it. In rice plants, shoot branching is the result of a developmental hold of the lateral buds produced by the absence of auxin, which is transferred from the SAM. The lateral bud outgrowth might be controlled by the enhanced biosynthesis of a group of inhibitors (Foo et al., 2005). Auxin suppresses the bud outgrowth via at least two different pathways; one pathway requires the branching inhibitor encoded by dwarf10 (d10), whereas the other pathway is self-regulating and is independent of this branching inhibitor. The presence of d10, an ortholog of RAMOSUS1 (RMS1), DECREASED APICAL DOMINANCE1 (DAD1) and MORE AXILLARY BRANCHING4 (MAX4)in rice and encodes the carotenoid cleavage dioxygenases, could be crucial for the regulation of the branching inhibitor pathway (Arite et al., 2007). Tillering is one of the most important components affecting the rice yield, and there is a long history of its study. Tillering is controlled by a two-step process of axillary meristem initiation and dormancy. The axillary meristem initiation is strongly dominated by the LAX PANICLE 1 pathway, whereas dormancy is clearly controlled by auxin and cytokinin in rice (Reviewed in Zhang and Yuan, 2014 and Reviewed in Pautler et al., 2013). Ran (Ras-related nuclear) was identified as a conserved eukaryotic GTPase. The over-expression analysis of Ran1 has shown a stimulating hypersensitivity to the exogenous auxins resulting in an increased number of tillers in transgenic rice plants (Wang et al., 2006). In addition, the phenotypes of OsmiR393-overexpression in rice are caused by the hyposensitivity to the auxin signal due to the decreased expression levels of two auxin receptor genes (RICETRANSPORT INHIBITOR RESPONSE 1 (OsTIR1) and AUXIN SIGNALING F-BOX 2(OsAFB2)), also leading to increased tiller numbers. Subsequently, the over-expression of OsmiR393 suppresses the expression of an auxin transporter
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(OsAUX1) and the tillering inhibitor (RICE TEOSINTE BRANCHED 1(OsTB1)) genes. Finally, a gene chain beginning with OsmiR393 to rice tillering, maybe from OsTIR1 and OsAFB2 to OsAUX1, affects the transportation of auxin, and OsTB1, which resulted in the regulation of tillering (Xia et al., 2012). In the rice genome, the LAXPANICLE (LAX), SMALL PANICLE (SPA) and MONOCULM 1 (MOC1) genes are also responsible for the regulation of the axillary meristem creation and the shoot branching (tiller) (Komatsu et al., 2003). A basic helix-loop-helix transcription factor is encoded by LAX, which is expressed into the boundary of SAM and the region of new meristem growth. LAX is a major factor in the formation of axillary meristems during morphogenesis in rice plants (Komatsu et al., 2003). At least seven homologs of the PIN (PIN-Formed, polar auxin transporter) gene have been characterised in the rice genome (Xu et al., 2005 and Morita and Kyozuka, 2004). Except for OsPIN1, the exact role of the other PIN genes in rice and their function in the regulation of the tiller growth remain unclear and must be determined in future studies (Xu et al., 2005).
2.1.2 Auxin and panicle formation in rice Two meristems, a primary SAM and the root meristem, are the primary axis of organogenesis in plants. The primary SAM generates several axillary meristems that become the panicle branches. The SAM of the panicle branches acts as the primary SAM and continuously produces higher-order axillary meristems.
The primary meristem of a panicle (inflorescence meristem) produces the rachis and the lateral meristems (also called the primary and secondary branching meristems) that will give rise to the primary branch axis. Finally, the lateral buds develop into the branching meristem, the spikelet meristem that differentiates the glumes and, subsequently, the floret meristem (Kurakawa et al., 2007); therefore, the panicles, panicle branches and lateral spikelets are created as axillary meristems in rice plants. From an agronomic viewpoint, the grain yield is normally supplied by the initial tillers and certain early secondary tillers, whereas the tertiary and next secondary tillers contribute only a small portion. In breeding programs, there is an interest in breeding rice plants with fewer and larger panicles to generate high yields (Reviewed in Khush, 2001). Thus, to increase the rice yield, the axillary bud activity should be inhibited in a timely manner via genetic and hormonal manipulation. Tillering and panicle formation share extensive similarities because they both engage with the apical growth and branching. Hence, analogous regulatory mechanisms could contribute to both of the processes.
The final plant
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architecture and panicle size are the products of a balance between the apical dominance and the branching at different levels. Cytokinin has been elucidated as a promoter of branching, resulting in increased spikelet numbers. Auxin provided by the primary shoot apex suppresses the axillary bud growth; however, CK reduces the inhibition and leads to the outgrowth of lateral branches (Taiz and Zeiger, 2006). However, whether auxinplays any role in the panicle size remains to be clarified.
3
Auxin/Cytokinin crosstalk and other hormones in SAM
The function of SAM relies on the combination of several hormones and their interactions (Fig. 4). Recent findings have suggested that the effects of high CK signalling on the stem cell activity are crucial for the preservation of the meristem cells. However, the initiation of certain organ development has been reported using an accurate balance between the divergent effects of CK on auxin (Sablowski, 2011). CK regulates the auxin biosynthesis conversely. The control of the CK-signalling pathway activity by auxin is mediated by the transcriptional modulation of its signal transduction. However, CK has shown feedback to the auxin activity by the conversion of the AUX/IAA genes expression involved in suppressing the auxin signalling pathway. Thus, CK directly affects the auxin diffusion mediated by the PIN family (auxin efflux carriers), whose expression is controlled by the auxin signalling pathway (Ruzicka et al., 2009 and Ioio et al., 2008). Recently, it has been reported that CK affects the adequate apicalbasal gynoecium differential patterning in Arabidopsis in an analogous manner to the suppression of the polar auxin transport, and a relationship between both of the hormones in this process has been suggested (Zuniga-Mayo et al., 2014 and Marhavy et al., 2011). A range of CKs led to enhanced auxin synthesis in young leaves, the shoot apex and the root system. This opposing effect was increased in the CK-hypersensitive-ARR mutant arr3, arr4, arr5, and arr6. Treatment of the CK-insusceptible fourfold AHP mutant ahp1, ahp2, ahp3 and ahp4 caused a decrease in the IAA biosynthesis, signifying that the correlation between the CK signalling and the auxin synthesis cannot be straightforward (Jones et al., 2010). An accumulation of the auxin activates organ initiation; however, auxin reduction surrounding the organs produces inhibitory fields that are assumed sufficient to maintain the plant phyllotaxis pattern.
The intercellular movement of the CK-signalling inhibitor ARABIDOPSIS HISTIDINE
PHOSPHOTRANSFER PROTEIN 6 (AHP6) is generated directly downstream of auxin and is involved in regulating the phyllotactic patterns in Arabidopsis. The AHP6-based fields created patterns of CK signalling in the meristem that involved the robustness of the phyllotaxis through the signal of a temporal sequence on the organ initiation. Finally, it has been suggested that two different hormonebased fields may be essential to achieve temporal precision during the arrangement of repetitive
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structures at the SAM, thus indicating an original mechanism for providing robustness to a dynamic developmental system (Besnard et al., 2014). The activity of CK and auxin directly congregates on the promoters of the ARR7 and ARR15 genes, two negative regulators of the CK signalling, and plays important meristematic roles. However, the expression of ARR7 and ARR15 is induced by CK in the SAM and is negatively affected by auxin, which is to a certain extent, mediated by the AUXIN RESPONSE FACTOR5/MONOPTEROS (MP) transcription factor in Arabidopsis (Reviewed in Zhao et al., 2010 and Leibfried et al., 2005). The CLV3 and CLV1 signals suppress the expression of WUS to a limited region inside of the corpus in Arabidopsis (Khurana et al., 2005). AS1 and AS2 are expressed in the stem cells of the Arabidopsis primordium and have a stimulatory effect (Fig. 4) (Cairney, 2007). The negative relationship between the SHOOT MERISTEMLESS (STM) and these two genes maintain the SAM/primordium boundary (Depuydt et al., 2008). The STM positively regulates IPT7 and negatively regulates GA20 oxidase (the enzymes involved in the CK and gibberellins (GA) biosynthesis) in the organ boundary areas of Arabidopsis (Reviewed in Fambrini and Pugliesi, 2013, Hay et al., 2006 and Ogas et al., 1999). CK promotes the expression of ARR7 and ARR15 via a STM-dependent pathway in Arabidopsis (Fig. 4). The negative regulation of WUS by these genes is crucial for stem cell formation (Reviewed in Fambrini and Pugliesi, 2013 and Leibfried et al., 2005). Auxin also interacts with the GAs, another group of hormones in the SAM; furthermore, auxin can activate the ethylene-dependent responses. Recently, it has been suggested that ethylene plays an important role in limiting the cell division in the Quiescent Centre (QC) of the root (Ortega-Martinez et al., 2007, Stepanova et al., 2007), but it is unclear whether it plays a similar role in limiting cell division in the CZ of the SAM. The additive or synergistic interactions of the auxin and brassinosteroids (BR) affects the dynamic behaviour of the SAM (Vandenbussche et al., 2013 and Belkhadir and Chory, 2006). The activation of the DR5 reporters is a specific response of BR to the auxin, which is diminished by the disruption of the BR signalling in Arabidopsis (Mouchel et al., 2006, Bao et al., 2004 and Nakamura et al., 2003). BR signalling is blocked in the dwarf plants phenotype, which can be recovered artificially; however, the expression of this signal in the epidermis is essential and is sufficient for the plant recovery. The priority of the epidermal cell layers in mediating the BR response asserts the “tensile limited growth” patterns (Kutschera, 2008). Based on this pattern, the total growth of the plants shows an equilibration between the extensibility of the superficial layers and the growth promoting turgor strengths. The possible connections of the layer specific responses have been strengthened by studies that have shown a restricted ability of BR for intercellular movement (Symons and Reid, 2004) and epidermally concentrated patterns of auxin transportation in the SAM (Reinhardt et al., 2003). The GA20- and GA3-oxidases are classes of enzymes that are controlled by the
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concentration of GA, and they are essential for GA biosynthesis. Additionally, GA deactivation is controlled via the GA2- oxidases. These classes of enzymes are produced by a family of genes, some of which are expressed principally in the SAM of Arabidopsis.
The beginning of the GA2-oxidases
biosynthesis occurs at the central meristem and is limited to the young organs; however, the enzymes involved in the deactivation of GA are expressed in the base of SAM (Hu et al., 2008, Rieu et al., 2008 and Jasinski et al., 2005). In the seedling stage of Arabidopsis, under auxin treatment, the expression of the GA oxidases by activating or deactivating roles has been confirmed. Among the GA oxidases, at least GA20ox1, GA20ox2, and GA20ox4 are expressed in the SAM; consequently, they could be targets of auxin signalling in the SAM (Frigerio et al., 2006). These GA oxidases have been encoded by the SemiDwarf-1(SD1) gene in rice (Ashikari et al., 2002). A wide range of genes, such as OsMADS1, plays important roles in modulating the expression of the shoot meristem, auxin and CK-mediated signalling events in rice; in addition, a combination of genes are regulated by OsMADS1 involved in developing the rice panicles. The suppression of OsMADS34, a LOFSEP gene, and the induction of the OsMADS55 expression, the identical gene involved in the SHORT VEGETATIVE PHASE-like floret meristem, confirmed its important role in the simplification of the spikelet to floret meristem transition. OsMADS1 is also involved in the direct regulation of transcription factor genes, such as OsHB4 (a homeo domain Leu zipper member), OsBLH1 (a BEL-like homeodomain member), OsKANAD12, OsKANAD14 and OsETTIN2, which illustrates its function in meristem maintenance, determinacy and lateral organ initiation and development. Overall, OsMADS1 has been shown to function in balancing the meristem growth, the lateral organ differentiation and determinacy by promoting the auxin transport, signalling, and auxin reliant expression and its direct suppression of three CK type-A OsRRs (Khanday et al., 2013). Moreover, the interaction of CK-auxin is included in the predominant shoot apex growth, which hinders the axillary bud outgrowth. FON2 and FON4, orthologs of CLV3, encode a secreted protein containing a CLE domain, which is localised at the SAM in rice plants. The function of FON2 and FON4 depends on the action of the FON1, ortholog of CLV1 (Chu et al., 2006 and Suzaki et al., 2006). The Log gene creates a region with high levels of CK/GA in the CZ of the SAM in rice.
Furthermore, the activation of the organ initiation by auxin as a mobile signal in meristem tissues has been established in the past decade (Braun et al., 2008); however, the characteristics of auxin transportation and its incorporation into the auxin biosynthesis and other hormone signalling during the organisation of cell activation and differentiation remain undiscovered and a challenge for the future.
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4
Conclusion
Various factors, including hormones, govern the remaining pluripotent SAM cells and lead to the formation of the different organs. The interaction of CK and auxin involved in the plant growth and organ formation has been widely considered. The critical roles of CK and auxin in the cell proliferation and new organ creation have been known for a long time. The cell destiny in particular tissues, which can be differentiated to a new shoot or root, is controlled by the ratio between these two hormones. Auxins have been known for their significant roles in establishing the leaf primordia and vascular elements; however, it appears that GAs and BR have a smaller effect on the differentiation pattern of the SAM compared with the other factors. Normal SAM can be formed without a significant activity of these hormones; however, it appears that these hormones are responsible for organogenesis and the maintenance of the SAM cells. Alternatively, understanding the interactions between auxin and CK is essential for controlling the developmental processes, such as the formation and maintenance of SAM, which are key factors for establishing the entire plant body. In the SAM, the CKs promote the proliferation of the stem cells and suppress the stem cell differentiation, whereas auxin plays a role in organ primordium initiation via the inhibition of the CK biosynthesis. Over the past decade, the studies on the hormones, their function and signalling in the plants have primarily focused on an analysis of the mutants of the genes involved in their synthesis, the signalling component, their transportation and the encoding receptors. Although studies have been performed on the different functions and aspects of the gene family members, an understanding of the feedback regulation of the CK and auxin pathways remains complicated. To completely understand the mechanism of CK, auxin and SAM signalling, it is essential to examine the involved genes of the monocotyledons and to evaluate the results by a comparison with dicotyledonous plants, such as Arabidopsis. In the future, it will be interesting not only to identify the genes in the biosynthetic pathway but also to study their function and understand the reason for the multiple pathways for auxin and CK biosynthesis. Furthermore, an investigation into whether there are any changes in the CK and auxin biosynthesis signalling pathways of the meristem cells in response to different conditions will be of interest.
5
Acknowledgements
The authors wish to acknowledge the Long-Term Research Grant Scheme (LRGS), Food Security project, Ministry of Higher Education, Malaysia, for the financial support.
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6
References
Anantharaman, V. and Aravind, L., 2001. The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci. 26, 579582. Arai, Y., Kawaguchi, M., Syono, K. and Ikuta, A., 2004. Partial purification of an enzyme hydrolyzing indole-3-acetamide from rice cells. J Plant Res. 117, 191-198. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H. and Kyozuka, J., 2007. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51, 1019-1029. Asakura, Y., Hagino, T., Ohta, Y., Aoki, K., Yonekura-Sakakibara, K., Deji, A., Yamaya, T., Sugiyama, T. and Sakakibara, H., 2003. Molecular characterization of His-Asp phosphorelay signaling factors in maize leaves: implications of the signal divergence by cytokinin-inducible response regulators in the cytosol and the nuclei. Plant Mol Biol. 52, 331-341. Ashikari, M., Sasaki, A., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Datta, S., Ishiyama, K., Saito, T., Kobayashi, M. and Khush, G.S., 2002. Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice 'green revolution'. Breed Sci. 52, 143-150. Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H. and Matsuoka, M., 2005. Cytokinin oxidase regulates rice grain production. Science. 309, 741-745. Attia, K.A., Abdelkhalik, A.F., Ammar, M.H., Wei, C., Yang, J., Lightfoot, D.A., El-Sayed, W.M. and ElShemy, H.A., 2009. Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice. Curr Iss Mol Biol. 11, I29.
Page 20 of 45
Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T. and Yang, Z., 2004. Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134, 1624-1631. Beemster, G.T.S. and Baskin, T.I., 2000. STUNTED PLANT 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol. 124, 1718-1727. Belkhadir, Y. and Chory, J., 2006. Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science. 314, 1410-1411. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G. and Friml, J., 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 115, 591–602. Besnard, F., Refahi, Y., Morin, V., Marteaux, B., Brunoud, G., Chambrier, P., Rozier, F., Mirabet, V., Legrand, J. and Laine, S., 2014. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature. 505, 417-424. Beveridge, C.A., 2006. Axillary bud outgrowth: sending a message. Curr Opin Plant Biol. 9, 35-40. Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O'Connor, D., Grotewold, E. and Hake, S., 2012. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26, 16851690. Brandstatter, I. and Kieber, J.J., 1998. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell. 10, 1009-1019. Braun, N., Wyrzykowska, J., Muller, P., David, K., Couch, D., Perrot-Rechenmann, C. and Fleming, A.J., 2008. Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell
Page 21 of 45
division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell. 20, 2746–2762. Capron, A., Chatfield, S., Provart, N. and Berleth, T., 2009. Embryogenesis: pattern formation from a single cell. The Arabidopsis Book/American Society of Plant Biologists 7. Cho, S.-H., Yoo, S.-C., Zhang, H., Lim, J.-H. and Paek, N.-C., 2014. Rice NARROW LEAF1 Regulates Leaf and Adventitious Root Development. Plant Mol Biol Rep. 32, 270-281. Chu, H., Qian, Q., Liang, W., Yin, C., Tan, H., Yao, X., Yuan, Z., Yang, J., Huang, H. and Luo, D., 2006. The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant physiol. 142, 1039-1052. D'Agostino, I.B., Deruere, J. and Kieber, J.J., 2000. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124, 1706-1717. Depuydt, S., Dolezal, K., Van Lijsebettens, M., Moritz, T., Holsters, M. and Vereecke, D., 2008. Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol. 146, 1267-1281. Dievart, A., Coudert, Y., Gantet, P., Pauluzzi, G., Puig, J., Fanchon, D., Ahmadi, N., Courtois, B., Guiderdoni, E. and Perin, C., 2013. Dissecting the biological bases of traits of interest in rice: Architecture and development of the root system. Cah Agric. 22, 475-483. Du, L., Jiao, F., Chu, J., Jin, G., Chen, M. and Wu, P., 2007. The two-component signal system in rice (Oryza sativa L.): A genome-wide study of cytokinin signal perception and transduction. Genomics. 89, 697-707.
Page 22 of 45
El-Showk, S., Ruonala, R. and Helariutta, Y., 2013. Crossing paths: cytokinin signalling and crosstalk. Development. 140, 1373-1383. Fambrini, M. and Pugliesi, C., 2013. Usual and unusual development of the dicot leaf: involvement of transcription factors and hormones. Plant Cell Rep. 1-24. Foo, E., Bullier, E., Goussot, M., Foucher, F., Rameau, C. and Beveridge, C.A., 2005. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell. 17, 464474. Frigerio, M., Alabadi, D., Perez-Gomez, J., Garcia-Carcel, L., Phillips, A.L., Hedden, P. and Blazquez, M.A., 2006. Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142, 553–563. Friml, J., 2003. Auxin transport—shaping the plant. Curr Opin Plant Biol. 6, 7–12. Fujino, K., Matsuda, Y., Ozawa, K., Nishimura, T., Koshiba, T., Fraaije, M.W. and Sekiguchi, H., 2008. NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genomics. 279, 499507. Gattolin, S., Alandete-Saez, M., Elliott, K., Gonzalez-Carranza, Z., Naomab, E., Powell, C. and Roberts, J.A., 2006. Spatial and temporal expression of the response regulators ARR22 and ARR24 in Arabidopsis thaliana. J Exp Bot. 57, 4225-4233. Giulini, A., Wang, J. and Jackson, D., 2004. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature. 430, 1031-1034. Gupta, S. and Rashotte, A.M., 2012. Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep. 31, 801-812.
Page 23 of 45
Haberer, G. and Kieber, J.J., 2002. Cytokinins. New insights into a classic phytohormone. Plant Physiol. 128, 354-362. Hass, C., Lohrmann, J., Albrecht, V.n., Sweere, U., Hummel, F., Yoo, S.D., Hwang, I., Zhu, T., Schufer, E. and Kudla, J.r., 2004. The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J. 23, 3290-3302. Hay, A., Kaur, H., Phillips, A., Hedden, P., Hake, S. and Tsiantis, M., 2002. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol. 12, 1557-1565. Hay, A., Barkoulas, M. and Tsiantis, M., 2006. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development. 133, 3955-3961. Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A. and Meyerowitz, E.M., 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 15, 1899-1911. Higuchi, M., Pischke, M., nen, A.M.h., Miyawaki, K., Hashimoto, Y., Seki, M., Kobayashi, M., Shinozaki, K., Kato, T. and Tabata, S., 2004. In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci U S A. 101, 8821-8826. Hirano, K., Aya, K., Hobo, T., Sakakibara, H., Kojima, M., Shim, R.A., Hasegawa, Y., Ueguchi-Tanaka, M. and Matsuoka, M., 2008. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol. 49, 1429-1450.
Page 24 of 45
Hirose, N., Makita, N., Kojima, M., Kamada-Nobusada, T. and Sakakibara, H., 2007. Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol. 48, 523-539. Horak, J., Grefen, C., Berendzen, K., Hahn, A., Stierhof, Y.-D., Stadelhofer, B., Stahl, M., Koncz, C. and Harter, K., 2008. The Arabidopsis thaliana response regulator ARR22 is a putative AHP phosphohistidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol. 8, 77. Hosoda, K., Imamura, A., Katoh, E., Hatta, T., Tachiki, M., Yamada, H., Mizuno, T. and Yamazaki, T., 2002. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell. 14, 2015-2029. Hu, J., Mitchum, M.G., Barnaby, N., Ayele, B.T., Ogawa, M., Nam, E., Lai, W.-C., Hanada, A., Alonso, J.M. and Ecker, J.R., 2008. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell. 20, 320-336. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J. and Fu, X., 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet. 41, 494-497. Hutchison, C.E. and Kieber, J.J., 2002. Cytokinin signaling in Arabidopsis. Plant Cell. 14, S47-S59. Hwang, I., Chen, H.-C. and Sheen, J., 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 129, 500-515. Hwang, I. and Sheen, J., 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature. 413, 383-389.
Page 25 of 45
Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Kiba, T., Ueguchi, C., Sugiyama, T. and Mizuno, T., 1999. Compilation and characterization of Arabiopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40, 733-742. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K. and Kakimoto, T., 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 409, 1060-1063. Ioio, R.D., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M.T., Aoyama, T., Costantino, P. and Sabatini, S., 2008. A genetic framework for the control of cell division and differentiation in the root meristem. Science. 322, 1380-1384. Ito, Y. and Kurata, N., 2006. Identification and characterization of cytokinin-signalling gene families in rice. Gene. 382, 57-65. Itoh, J.-I., Kitano, H., Matsuoka, M. and Nagato, Y., 2000. SHOOT ORGANIZATION genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell. 12, 2161-2174. Itoh, J.-I., Nonomura, K.-I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H. and Nagato, Y., 2005. Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46, 23-47. Jain, M., Kaur, N., Garg, R., Thakur, J.K., Tyagi, A.K. and Khurana, J.P., 2006. Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa L.). Funct Integr Genomics.. 6, 47-59. Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P. and Tsiantis, M., 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol. 15, 1560-1565.
Page 26 of 45
Jeon, J. and Kim, J., 2013. Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant physiol. 161 408–424 Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novak, O., Ku, S.-J., Cho, C., Lee, D.J., Lee, E.-J. and Strnad, M., 2010. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem. 285, 23371-23386. Jin, J., Huang, W., Gao, J.-P., Yang, J., Shi, M., Zhu, M.-Z., Luo, D. and Lin, H.-X., 2008. Genetic control of rice plant architecture under domestication. Nat genet. 40, 1365-1369. Jones, B., Gunneras, S.A., Petersson, S.V., Tarkowski, P., Graham, N., May, S., Dolezal, K., Sandberg, G. and Ljung, K., 2010. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell. 22, 2956-2969. Kawakatsu, T., Taramino, G., Itoh, J.I., Allen, J., Sato, Y., Hong, S.K., Yule, R., Nagasawa, N., Kojima, M. and Kusaba, M., 2009. PLASTOCHRON3/GOLIATH encodes a glutamate carboxypeptidase required for proper development in rice. Plant J. 58, 1028-1040. Kerstetter, R.A. and Hake, S., 1997. Shoot meristem formation in vegetative development. Plant Cell. 9, 1001. Khanday, I., Yadav, S.R. and Vijayraghavan, U., 2013. Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol. 161, 1970-1983. Khurana, J.P., Tripathi, L., Kumar, D., Thakur, J.K. and Malik, M.R., 2005. Cell Differentiation in Shoot Meristem: A Molecular Perspective, Plant biotechnology and molecular markers. Springer, pp. 366-385.
Page 27 of 45
Khush, G.S., 2001. Green revolution: the way forward. Nat Rev Genet. 2, 815-822. Kiba, T., Taniguchi, M., Imamura, A., Ueguchi, C., Mizuno, T. and Sugiyama, T.,1999. Differential expression of genes for response regulators in response to cytokinins and nitrate in Arabidopsis thaliana. Plant Cell Physiol. 40, 767-771. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G. and Hwang, I., 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci U S A. 103, 814-819. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K. and Kyozuka, J., 2003. LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci. 100, 1176511770. Kramer, E.M. and Bennett, M., 2006. Auxin transport: a field in flux. Trends Plant Sci. 11, 382–386. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., Sakakibara, H. and Kyozuka, J., 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 445, 652-655. Kushwaha, H.R., Singla-Pareek, S.L. and Pareek, A., 2014. Putative osmosensor-OsHK3b-a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J Biomol Struct Dyn. 32, 1318-1332. Kutschera, U., 2008. The pacemaker of plant growth. Trends Plant Sci. 13, 105-107. Laplaze, L., Benkova, E., Casimiro, I., Maes, L., Vanneste, S., Swarup, R., Weijers, D., Calvo, V., Parizot, B. and Herrera-Rodriguez, M.B.a., 2007. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell. 19, 3889-3900.
Page 28 of 45
Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J. and Lohmann, J.U., 2005. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature. 438, 1172-1175. Leyser, O., 2006. Dynamic integration of auxin transport and signaling. Curr Biol. 16, 424–433. Li, P., Wang, Y., Qian, Q., Fu, Z., Wang, M., Zeng, D., Li, B., Wang, X. and Li, J., 2007. LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Res. 17, 402-410. Lohrmann, J., Buchholz, G., Keitel, C., Sweere, U., Kircher, S., Baurle, I., Kudla, J., Schufer, E. and Harter, K., 1999. Differential Expression and Nuclear Localization of Response Regulator-Like Proteins from Arabidopsis thaliana1. Plant Biol. 1, 495-505. Lomin, S.N., Krivosheev, D.M., Steklov, M.Y., Osolodkin, D.I. and Romanov, G.A., 2012. Receptor properties and features of cytokinin signaling. Acta Naturae. 4, 31. Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K., 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature. 379, 66-69. Marhavy, P., Bielach, A., Abas, L., Abuzeineh, A., Duclercq, J., Tanaka, H., Parezova, M., Petrasek, J., Friml, J. and Kleine-Vehn, J., 2011. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell. 21, 796-804. Mason, M.G., Jha, D., Salt, D.E., Tester, M., Hill, K., Kieber, J.J. and Eric Schaller, G., 2010. Type-B response regulators and ARR12 regulate expression of AtHKT1; 1 and accumulation of sodium in Arabidopsis ARR1 shoots. Plant J. 64, 753-763. McSteen, P. and Leyser, O., 2005. Shoot branching. Annu. Rev. Plant Biol. 56, 353-374. Morita, Y. and Kyozuka, J., 2004. Identification of rice PIN homologs. Rice Genet Newsl. 21, 87-88.
Page 29 of 45
Morita, Y. and Kyozuka, J., 2007. Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. Plant Cell Physiol. 48, 540-549. Mouchel, C.l.F., Osmont, K.S. and Hardtke, C.S., 2006. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature. 443, 458-461. Murray, J.A.H., Jones, A., Godin, C. and Traas, J., 2012. Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell. 24, 3907-3919. Nakamura, A., Higuchi, K., Goda, H., Fujiwara, M.T., Sawa, S., Koshiba, T., Shimada, Y. and Yoshida, S., 2003. Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol. 133, 1843-1853. Nakamura, A., Umemura, I., Gomi, K., Hasegawa, Y., Kitano, H., Sazuka, T. and Matsuoka, M., 2006. Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. Plant J. 46, 297-306. Nemhauser, J. and Chory, J., 2002. Photomorphogenesis. The Arabidopsis Book/American Society of Plant Biologists. 1. Nieminen, K., Immanen, J., Laxell, M., Kauppinen, L., PTarkowski, Dolezal, K., htiharju, S.T., Elo, A., Decourteix, M. and Ljung, K., 2008. Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA. 105, 20032-20037. Nishimura, C., Ohashi, Y., Sato, S., Kato, T., Tabata, S. and Ueguchi, C., 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16, 1365-1377.
Page 30 of 45
Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C., 1999. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Nat Acad Sci. 96, 13839-13844. Ortega-Martinez, O., Pernas, M., Carol, R.J. and Dolan, L., 2007. Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science. 317, 507-510. Park, W.J., Kriechbaumer, V., Muller, A., Piotrowski, M., Meeley, R.B., Gierl, A. and Glawischnig, E., 2003. The nitrilase ZmNIT2 converts indole-3-acetonitrile to indole-3-acetic acid. Plant Physiol. 133, 794-802. Pautler, M., Tanaka, W., Hirano, H.-Y. and Jackson, D., 2013. Grass meristems I: shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant Cell Physiol. 54, 302312. Qi, J., Qian, Q., Bu, Q., Li, S., Chen, Q., Sun, J., Liang, W., Zhou, Y., Chu, C. and Li, X., 2008. Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol. 147, 1947-1959. Ramireddy, E., 2009. Functional characterization of B-type response regulators of Arabidopsis thaliana. Dissertation, Freie Universitat Berlin, Berlin. Rashotte, A.M., Carson, S.D.B., To, J.P.C. and Kieber, J.J., 2003. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 132, 1998-2011. Rashotte, A.M., Mason, M.G., Hutchison, C.E., Ferreira, F.J., Schaller, G.E. and Kieber, J.J., 2006. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a twocomponent pathway. Proc Natl Acad Sci. 103, 11081-11085.
Page 31 of 45
Reinhardt, D., Mandel, T. and Kuhlemeier, C., 2000. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell. 12, 507–519. Reinhardt, D., Pesce, E., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C., 2003. Regulation of phyllotaxis by polar auxin transport. Nature. 426, 255–260. Riefler, M., Novak, O., Strnad, M. and lling, T.S., 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell. 18, 40-54. Rieu, I., Eriksson, S., Powers, S.J., Gong, F., Griffiths, J., Woolley, L., Benlloch, R., Nilsson, O., Thomas, S.G. and Hedden, P., 2008. Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell. 20, 2420-2436. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H., 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science. 283, 1541-1544. Roef, L. and Van Onckelen, H., 2010. Cytokinin regulation of the cell division cycle, Plant Hormones. Springer, pp. 241-261. Ruzicka, K., Simaskova, M., Duclercq, J., Petrasek, J., Zazimalova, E., Simon, S., Friml, J., Van Montagu, M.C.E. and Benkova, E., 2009. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci. 106, 4284-4289. Sablowski, R., 2011. Plant stem cell niches: from signalling to execution. Curr Opin Plant Biol. 14, 4-9. Sakai, H., Aoyama, T., Bono, H. and Oka, A., 1998. Two-component response regulators from Arabidopsis thaliana contain a putative DNA-binding motif. Plant Cell Physiol. 39, 1232-1239.
Page 32 of 45
Sakai, H., Aoyama, T. and Oka, A., 2000. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703-711. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S. and Oka, A., 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science. 294, 1519-1521. Sakakibara, H., 2006. Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol. 57, 431449. Sakakibara, H., Takei, K. and Hirose, N., 2006. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 11, 440-448. Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S. and Matsuoka, M., 2001. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 15, 581-590. Sakamoto, T., Sakakibara, H., Kojima, M., Yamamoto, Y., Nagasaki, H., Inukai, Y., Sato, Y. and Matsuoka, M., 2006. Ectopic expression of KNOTTED1- like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol Comm. 142, 54-62. Sassi, M. and Vernoux, T., 2013. Auxin and self-organization at the shoot apical meristem. J Exp Bot. 64, 2579-2592. Schaller, G.E., 2000. Histidine kinases and the role of two-component systems in plants. Adv Bot Res. 32, 109–148. Schaller, G.E., Kieber, J.J. and Shiu, S.-H., 2008. Two-component signaling elements and histidyl-aspartyl phosphorelays. The Arabidopsis Book/American Society of Plant Biologists. 6.
Page 33 of 45
Sieberer, T. and Leyser, O., 2006. Plant science: auxin transport, but in which direction? Science. 312, 858–860. Skoog, F. and Miller, C., 1957. Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol. 11, 118-131. Song, Y., Wang, L. and Xiong, L., 2009. Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta. 229, 577-591. Song, Y. and Xu, Z.-F., 2013. Ectopic overexpression of an AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) gene OsIAA4 in rice induces morphological changes and reduces responsiveness to auxin. Int J Mol Sci. 14, 13645-13656. Srivastava, L.M., 2002. Plant growth and development: hormones and environment, Access Online via Elsevier. Steeves, T.A. and Sussex, I.M., 1989. Patterns in plant development. Cambridge University Press. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.-Y., Dolezal, K., Schlereth, A., Jurgens, G. and Alonso, J.M., 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 133, 177-191. Stepanova, A.N., Yun, J., Likhacheva, A.V. and Alonso, J.M., 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 19, 2169-2185. Sticklen, M.B. and Oraby, H.F., 2005. Invited review: shoot apical meristem: A Sustainable explant for genetic transformation of cereal crops. In Vitro Cell Dev Biol Plant. 41, 187–200.
Page 34 of 45
Su, Y.-H., Liu, Y.-B. and Zhang, X.-S., 2011. Auxin-cytokinin interaction regulates meristem development. Mol Plant. 4, 616-625. Sugawara, S., Hishiyama, S., Jikumaru, Y., Hanada, A., Nishimura, T., Koshiba, T., Zhao, Y., Kamiya, Y. and Kasahara, H., 2009. Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Nat Acad Sci. 106, 5430-5435. Sun, L., Zhang, Q., Wu, J., Zhang, L., Jiao, X., Zhang, S., Zhang, Z., Sun, D., Lu, T. and Sun, Y., 2014. Two Rice Authentic Histidine Phosphotransfer Proteins, OsAHP1 and OsAHP2, Mediate Cytokinin Signaling and Stress Responses in Rice. Plant Physiol. 165, 335-345. Suzaki, T., Toriba, T., Fujimoto, M., Tsutsumi, N., Kitano, H. and Hirano, H.-Y., 2006. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47, 1591-1602. Suzuki, T., Miwa, K., Ishikawa, K., Yamada, H., Aiba, H. and Mizuno, T., 2001. The Arabidopsis sensor Hiskinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42, 107-113. Swanson, R.V., Alex, L.A. and Simon, M.I., 1994. Histidine and aspartate phosphorylation: twocomponent systems and the limits of homology. Trends biochem sci. 19, 485-490. Symons, G.M. and Reid, J.B., 2004. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 21962206. Taiz, L. and Zeiger, E., 2006. Plant Physiology. 4th ed. Sinauer, Sunderland, MA. Tan, L., Li, X., Liu, F., Sun, X., Li, C., Zhu, Z., Fu, Y., Cai, H., Wang, X. and Xie, D., 2008. Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet. 40, 1360-1364.
Page 35 of 45
Tanaka, M., Takei, K., Kojima, M., Sakakibara, H. and Mori, H., 2006. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 45, 1028-1036. Taniguchi, M., Kiba, T., Sakakibara, H., Ueguchi, C., Mizuno, T. and Sugiyama, T., 1998. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429, 259-262. Tao, Y., Ferrer, J.-L., Ljung, K., Pojer, F., Hong, F., Long, J.A., Li, L., Moreno, J.E., Bowman, M.E. and Ivans, L.J., 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 133, 164-176. Thakur, J.K., Tyagi, A.K. and Khurana, J.P., 2001. OsIAA1, an Aux/IAA cDNA from rice, and changes in its expression as influenced by auxin and light. DNA Res. 8, 193-203. To, J.P., Haberer, G., Ferreira, F.J., Deruère, J., Mason, M.G., Schaller, G.E., Alonso, J.M., Ecker, J.R. and Kieber, J.J., 2004. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell. 16, 658-671. To, J.P.C. and Kieber, J.J., 2008. Cytokinin signaling: two-components and more. Trends Plant Sci. 13, 8592. Tsai, Y.-C., Weir, N.R., Hill, K., Zhang, W., Kim, H.J., Shiu, S.-H., Schaller, G.E. and Kieber, J.J., 2012. Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol. 158, 1666-1684. Tsuda, K., Ito, Y., Sato, Y. and Kurata, N., 2011. Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell. 23, 4368-4381.
Page 36 of 45
Ueguchi, C., Koizumi, H., Suzuki, T. and Mizuno, T., 2001. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42, 231-235. Vandenbussche, F., Callebert, P., Zadnikova, P., Benkova, E. and Van Der Straeten, D., 2013. Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. Am J Bot. 100, 215-225. Vernoux, T., Besnard, F. and Traas, J., 2010. Auxin at the Shoot Apical Meristem. Cold Spring Harb Perspect Biol. 2, 1-14. Vollbrecht, E., Reiser, L. and Hake, S., 2000. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development. 127, 3161-3172. Waller, F., Furuya, M. and Nick, P., 2002. OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol Biol. 50, 415-425. Wang, B., Chen, Y., Guo, B., Kabir, M.R., Yao, Y., Peng, H., Xie, C., Zhang, Y., Sun, Q. and Ni, Z., 2014. Expression and functional analysis of genes encoding cytokinin receptor-like histidine kinase in maize (Zea mays L.). Mol Genet Genomics. 1-12. Wang, X., Xu, Y., Han, Y., Bao, S., Du, J., Yuan, M., Xu, Z. and Chong, K., 2006. Overexpression of RAN1 in rice and Arabidopsis alters primordial meristem, mitotic progress, and sensitivity to auxin. Plant Physiol. 140, 91-101. Weijers, D., Sauer, M., Meurette, O., Friml, J., Ljung, K., Sandberg, G., Hooykaas, P. and Offringa, R., 2005. Maintenance of embryonic auxin distribution for apical–basal patterning by PIN-FORMEDdependent auxin transport in Arabidopsis. Plant Cell. 17, 2517–2526.
Page 37 of 45
Werner, T., Motyka, V., Laucou, V., Smets, R., Onckelen, H.V. and lling, T.S., 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 15, 2532-2550. West, A.H. and Stock, A.M., 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci. 26, 369-376. Wohlbach, D.J., Quirino, B.F. and Sussman, M.R., 2008. Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell. 20, 1101-1117. Woo, Y.-M., Park, H.-J., Suudi, M., Yang, J.-I., Park, J.-J., Back, K., Park, Y.-M. and An, G., 2007. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Mol Biol. 65, 125-136. Woodward, A.W. and Bartel, B., 2005. Auxin: regulation, action, and interaction. Ann Bot. 95, 707-735. Wright, A.D., Sampson, M.B., Neuffer, M.G., Michalczuk, L., Slovin, J.P. and Cohen, J.D., 1991. Indole-3acetic acid biosynthesis in the mutant maize orange pericarp, a tryptophan auxotroph. Science. 254, 998-1000. Xia, K., Wang, R., Ou, X., Fang, Z., Tian, C., Duan, J., Wang, Y. and Zhang, M., 2012. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PloS one. 7, e30039. Xu, M., Zhu, L., Shou, H. and Ping, W., 2005. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674–1681.
Page 38 of 45
Xu, Y., Zhang, S., Guo, H., Wang, S., Xu, L., Li, C., Qian, Q., Chen, F., Geisler, M. and Qi, Y., 2014. OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa. L). Plant J. 79, 106-117. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T. and Mizuno, T., 2001. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M. and Sazuka, T., 2007. Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol. 143, 1362-1371. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A. and Ori, N., 2005. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol. 15, 1566-1571. Yonekura-Sakakibara, K., Kojima, M., Yamaya, T. and Sakakibara, H., 2004. Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol. 134, 1654-1661. Yoshikawa, T., Ito, M., Sumikura, T., Nakayama, A., Nishimura, T., Kitano, H., Yamaguchi, I., Koshiba, T., Hibara, K.-I. and Nagato, Y., 2014. The rice FISH BONE gene encodes a tryptophan aminotransferase, which affects pleiotropic auxin-related processes. Plant J. Zadnikova, P. and Simon, R., 2014. How boundaries control plant development. Curr Opin Plant Biol. 17, 116-125. Zhang, D. and Yuan, Z., 2014. Molecular control of grass inflorescence development. Annu Rev Plant Biol. 65, 553-578.
Page 39 of 45
Zhao, Y., 2008. The role of local biosynthesis of auxin and cytokinin in plant development. Curr Opin Plant Biol. 11, 16-22. Zhao, Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D. and Chory, J., 2001. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science. 291, 306–309. Zhao, Z., Andersen, S.U., Ljung, K., Dolezal, K., Miotk, A., Schultheiss, S.J. and Lohmann, J.U., 2010. Hormonal control of the shoot stem-cell niche. Nature. 465, 1089-1092. Zhuang, X., Jiang, J., Li, J., Ma, Q., Xu, Y., Xue, Y., Xu, Z. and Chong, K., 2006. Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J. 48, 581-591. Zuniga-Mayo, V.M., Reyes-Olalde, J.I., Marsch-Martinez, N. and De Folter, S., 2014. Cytokinin treatments affect the apical-basal patterning of the Arabidopsis gynoecium and resemble the effects of polar auxin transport inhibition. Front Plant Sci. 5. Fig. 1 - Cytokinin signalling in rice. PM: Plasma membrane; NM: Nucleus membrane. The CHASE domain is positioned outside of the PM and binds CK (shown in red). The phosphoryl group is shown in the green circle. His and Asp are shown as H and D, respectively. The OsAHPs are shown with the green rectangle; modified from (El-Showk et al., 2013 and To and Kieber, 2008).
Fig. 2 - A schematic illustration of the cytokinin biosynthesis and activation pathways.Adenosine phosphate-isopentenyl-transferase (IPT) (1); CYP735A (2); Phosphatase (3); 5/- ribonucleotidephosphohydrolase (4); adenosine nucleosidase (5); Zeatinreductase (6); Purine nucleoside phosphorylase (7) Phosphorylation by
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Genes
Functions
References
adenosine kinase (8); modified from (Kurakawa et al., 2007, Sakakibara et al., 2006 and Sakamoto et al., 2006). Fig. 3 - Proposed tryptophan-dependent pathway of IAA biosynthesis in rice.The dotted arrows show the steps that are joined with the glucosinolate pathway. Modified from (Hirano et al., 2008 and Yamamoto et al., 2007)
Fig. 4 - A schematic molecular representation of the Auxin, CK, and Gibberellin (GA) interaction mechanisms in the regulation of meristem development in Arabidopsis (A) Modified from (Su et al., 2011) and rice (B).
Table 1- List of certain cytokinin signalling regulators
Page 41 of 45
WUSCHEL
Preserves undifferentiated stem cells and directly suppresses
(WUS)
a subgroup of the A form of the ARR genes; also act as a
(Leibfried et al., 2005)
regulator of the cytokinin signal in the negative response manner in Arabidopsis. This gene is homologous to OsWUS in rice. CKX
Reduces the cambial activity as a cytokinin signalling gene in
(Nieminen et al., 2008)
rice, maize and Arabidopsis IPT
Effective for the cambial growth and restricts the import of
(Tanaka et al., 2006)
cytokinins into the axillary bud in rice CHARK
Cytokinin receptor in rice
(Ito and Kurata, 2006)
OsARR2
Mediates a cytokinin signal, most likely through its NH2- (Dievart et al., 2013, Kim et al., terminal signal receiver domain, and transactivates ARR6, which is immediately responsive to the cytokinins.
2006 and Riefler et al., 2006)
Its
orthologous gene reduces the effects of AHK2, and AHK3 and mediates the leaf senescence activity in Arabidopsis OsHK2, 3, 4, 5 OsMADS1
Cytokinin receptor in rice Direct repression of three cytokinin A-type response
(Ito and Kurata, 2006) (Khanday et al., 2013)
regulators and regulates the meristem growth and the lateral organ development in rice OsARR6
A small panicle has been reported in transgenic rice plants
(Hirose et al., 2007)
that constitutively express OsARR6, a negative regulator of CK signalling
Page 42 of 45
Genes
Product Functions
References
Table 2 - Genes involved in the auxin biosynthesis, transport and signal transduction.
Page 43 of 45
OsAUX1
Auxin carrier inrice
(Xia et al., 2012)
LA1
Auxin transporter, engages in controlling the tiller angle, and
(Li et al., 2007)
suppresses auxin transportation in rice PGP
Auxin influx carrier in rice and Arabidopsis
(Xu et al., 2014 and Kramer and Bennett, 2006)
ARF
Transcription factor, inducer of auxin, expressed in coleoptiles,
(Attia et al., 2009 and
callus, and young panicles with weaker expression in leaves and
Waller et al., 2002)
roots, affects the vegetative development in rice Nal1
OsPIN1
Auxin transporter, causes stem elongation and adventitious root
(Cho et al., 2014 and Qi et
development in rice
al., 2008)
Auxin transporter and involved in controlling the tiller angle in
(Xu et al., 2005)
rice PROG1
Affects the tiller and panicle branch number and the yield of rice
(Jin et al., 2008 and Tan et
plants
al., 2008)
OsTIR1
auxin receptor genes in rice
(Xia et al., 2012)
OsYUCCA1
Exhibits an overproduction of IAA, expressed in nearly all of the
(Yamamoto et al., 2007)
organs and overlaps with the expression of a β-glucuronidase reporter gene regulated by the Auxin responsive DR5promoter in rice OsAGAP
Auxin transporter in rice
(Zhuang et al., 2006)
OsCOW1/
Auxin biosynthesis in rice
(Fujino et al., 2008 and
OsNAL7 OsNIT
Yamamoto et al., 2007) Auxin biosynthesis in rice
(Park et al., 2003)
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OsPID
Transporting auxin in rice
(Morita and Kyozuka, 2007)
OsARF1
Auxin response factor/Auxin signal transduction in rice
(Attia et al., 2009)
FISH
Auxin biosynthesis, transport and sensitivity; affects the
(Yoshikawa et al., 2014)
BONE (FIB)
pleiotropic auxin-related processes in rice
Page 45 of 45
S0925-4773(14)00068-9 http://dx.doi.org/doi: 10.1016/j.mod.2014.11.001 MOD 3317
To appear in:
Mechanisms of Development
Received date: Revised date: Accepted date:
15-4-2014 5-11-2014 14-11-2014
Please cite this article as: P. Azizi, M.Y. Rafii, M. Maziah, S.N.A. Abdullah, M.M. Hanafi, M.A. Latif, A.A. Rashid, M. Sahebi, Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice, Mechanisms of Development (2014), http://dx.doi.org/doi: 10.1016/j.mod.2014.11.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice P. Azizi1, M.Y. Rafii1, M. Maziah2, S. N. A. Abdullah3, M.M. Hanafi1, M.A. Latif1, A.A. Rashid4, M. Sahebi1
1
Laboratory of Food Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400
Serdang,Selangor, Malaysia. 2
Department of Biochemistry, Faculty of Biotechnology and BiomolecularScience, Universiti Putra
Malaysia, 43400 Serdang,Selangor, Malaysia. 3
Laboratory of Crop Science, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400 Serdang,
Selangor, Malaysia. 4
Department of Agriculture Technology, Faculty of Agriculture, Universiti Putra Malaysia, 43400
Serdang,Selangor, Malaysia.
Corresponding author: M.Y. Rafii [email protected] .
Highlights
Cytokinin has been elucidated as a promoter of branching, resulting in increased spikelet numbers in rice.
Page 1 of 45
Auxin provided by the primary shoot apex suppresses axillary bud growth; however, CK reduces the inhibition and leads to the outgrowth of lateral branches.
The decreased level of CK resulted in the increasing of apical dominance and represses the growth of axillary bud.
Graphical Abstract
Abstract
Page 2 of 45
Auxin and cytokinin regulate different critical processes involved in plant growth and environmental feedbacks. These plant hormones act either synergistically or antagonistically to control the organisation, formation and maintenance of meristem. Meristem cells can be divided to generate new tissues and organs at the locations of plant postembryonic development. The aboveground plant organs are created by the shoot apical meristem (SAM). It has been proposed that the phytohormone, cytokinin, plays a positive role in the shoot meristem function, promotes cell expansion and promotes an increasing size of the meristem in Arabidopsis, whereas it has the reverse effects in the root apical meristem (RAM). Over the last few decades, it has been believed that the apically derived auxin suppresses the shoot branching by inactivating the axillary buds.However, it has recently become clear that the mechanism of action of auxinis indirect and multifaceted. In higher plants, the regulatory mechanisms of the SAM formation and organ separation are mostly unknown. This study reviews the effects and functions of cytokinin and auxin at the shoot apical meristem. This study also highlights the merger of the transcription factor activity with the actions of cytokinin/auxin and their complex interactions with the shoot meristem in rice.
Keywords: Stem cells, Transcription factors, cell expansion, axillary buds.
Page 3 of 45
Contents Abstract ................................................................................................................................. 1 1 Introduction ................................................................................................................... 4 2 Hormonal Pathways required for SAM maintenance and functions ............................ 6 2.1
Cytokinin actions on the SAM ............................................................................... 6
2.1.1 2.2
Cytokinin signaling transduction in rice ......................................................... 8
Auxin signaling in the SAM................................. Error! Bookmark not defined.
2.2.1 2.2.2
Auxin and the shoot branching pattern (Tillering) in rice ............................ 14 Auxin and Panicle formation in rice ............. Error! Bookmark not defined.
3 4 5 6
Auxin/Cytokinin crosstalk and other hormones in SAM ............................................ 16 Conclusion .................................................................................................................. 19 Acknowledgements ..................................................................................................... 19 References ................................................................... Error! Bookmark not defined.
1
Introduction
The stem cells of plant meristems play different roles in the growth and development of new organs over the plant lifetime. All of the post-embryonically shaped organs and tissues are produced from pluripotent stem cells that exist in the growing tips of the plants, namely the shoot apical meristem (SAM) and the root apical meristem (RAM). The aboveground organs in plants are created by the SAM, whereas the belowground organs are formed through the RAM. In monocotyledons, most of the plant parts are generated from the SAM because the root system consists primarily of adventitious roots, with a small portion consisting of radicle. The mechanisms of SAM development during embryogenesis and maintenance and its roles in the postembryonic growth are the primary concern in plant developmental biology. Stem cells in the SAM are constantly selfrenewing, instinctive and can develop into all of the types of cells that form the shoot components (Itoh et al., 2000). For example, the leaf is the essential lateral organ and is repetitively derived from the SAM. The final leaf shape, the plastochron and the phyllotaxy are organised by the SAM in rice (Kawakatsu et al., 2009 and Heisler et al., 2005). Generally, the procedure of SAM formation during embryogenesis is divided in three phases. The first phase determines the axes during the beginning stage of embryogenesis. The next phase generates and senses regional information to locate the SAM inside of the embryo. The final phase is the SAM formation. Embryogenesis in monocots differs from that in other plants, such as Arabidopsis (Reviewd in Itoh et al., 2005), regarding several specific
Page 4 of 45
features. For example, several organs are specifically produced in rice involving the scutellum, epiblast and coleoptiles. Moreover, in the early stage of embryogenesis until the end of the globular steps, the rice embryo does not follow a stereotypical pattern of cell division, and the division directions are not fixed. In contrast, other cells have shown a stereotypical division pattern during the early stages of embryogenesis. In Arabidopsis, the cell lineage-related information may affect the specific location of SAM and other organs in the post-embryogenesis stages (Capron et al., 2009). However, because of the non-conserved cell divisions pattern, rice cells must detect their locations, which are created by externally or internally positional information independent of the cell lineage in the early stages of embryogenesis. In monocots, the SAM is formed laterally at the base of their single cotyledon. During the post-embryonic stages, various organs, including leaves, stems and axillary buds, are generated by the SAM while the indistinctive stem cell populations are maintained. The SAM of most of the angiosperms is planned into a central zone, containing gradually and continually dividing stem cells, and a peripheral zone, composed of the cells with the ability to rapidly divide and that can be integrated into the organ primordial (Reviewed in Zadnikova and Simon, 2014 and Kerstetter and Hake, 1997). The central region of the SAM in cereal crops is surrounded by two different dividing cell layers (L1 and L2), which tend to be taller and finger shaped. This region of the SAM includes three layers (L1, L2, and L3) in dicots (Reviewed in Sticklen and Oraby, 2005 and Steeves and Sussex, 1989). To date, different detailed aspects of the apical meristem have been considered. Auxin and cytokinin, as two plant growth regulators, play relatively essential roles in many features of plant development. Furthermore, the interaction between auxin and cytokinin is important for the regulation of a few developmental processes, such as the formation and maintenance of the meristem, which are crucial mechanisms for the establishment of the intact plant (Reviewed in Zhao, 2008, Ashikari et al., 2005, Giulini et al., 2004, Reinhardt et al., 2003 and Reinhardt et al., 2000). Cytokinin positively modulates cell division and proliferation in the shoot stem cell regions; in addition, the organising centre in the central region is a highly cytokinin sensitive area of the SAM (Reviewed in Murray et al., 2012, Riou-Khamlichi et al., 1999 and Skoog and Miller, 1957). The root and SAM patterning and lateral organ development are also regulated by auxin in the postembryonal development stages (Benkova et al., 2003). The importance of SAM inspires an increased focus on the effective mechanisms involved in its function and maintenance. In this study, we review the molecular mechanisms of cytokinin and auxin at the shoot apical meristem and highlight the merger of the transcription factor activity with the actions of cytokinin and auxin and their complex interactions with the shoot meristem in rice.
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2
Hormonal Pathways required for SAM maintenance and functions
Physiological studies have revealed the vital role of two phytohormones, cytokinins (CKs) and auxins, in the control of axillary bud growth. Generally, auxin is produced by the primary shoot apex cells, which inhibit the development of axillary buds; however, this inhibition is relieved by CK to enable the development of the lateral branches (Tanaka et al., 2006). Therefore, the growth of the axillary buds is controlled positively and negatively via the CKs and auxins, respectively.
2.1
Cytokinin actions on the SAM
Cytokinin plays roles in various aspects of plant growth, including leaf senescence, apical dominances, shoot meristem activity and formation, nutrient mobilisation, seed germination, and the response to stresses (Riefler et al., 2006, Werner et al., 2003 and Srivastava, 2002). Moreover, CK directly affects the lateral root founder cells to suppress the root initiation (Laplaze et al., 2007). The regulation of the CK activity is similar to other plant hormones in which the maintenance of the balance among its synthesis, degradation, inactivation, reactivation, and so on is required (Reviewed in Sakakibara, 2006). N6Isopentenyladenine (iP) and trans-Zeatin (tZ), which are common natural isoprenoid CKs, are originally the products of the methylerythritol phosphate (MEP) pathway, whereas a large portion of cis-Zeatin (Cz) is obtained from the mevalonate (MVA) pathway. ATP, ADP and AMP are converted to the iPRT, iPRDP, and iPRMP forms, respectively, by adenosine phosphate-isopentenyl-transferase (IPT). IPTs are encoded by a small gene family that includes at least eight members in rice plants (OsIPT1 to OsIPT8) (Sakamoto et al., 2006). Among these transcriptional factors, the expression of theOsIPT2 and OsIPT3 genes is induced by OSH1. The nucleotides entering the CK pathway are converted to tZ-nucleotides by CYP735A, whereas iP, tZ, dZ and cZ can be catabolised by the expression of the LONELY GUY (LOG) gene or by a function of adenosine nucleosidase in this pathway (Fig. 2) (Kurakawa et al., 2007 and Sakamoto et al., 2006). The LOG gene is expressed in the apical zone of the rice meristem tissue, which contains stem cells. Loss of function mutations in the LOG locus have been shown to reduce the meristemal cell number, and ultimately reduce the SAM size (Kurakawa et al., 2007); consequently, these plants formed small panicles with imperfect flowers. In maize, theKnotted-1 (Kn1) mutants have shown a smaller meristem size compared with the normal plants (Vollbrecht et al., 2000). The orthologs of kn1, STM in Arabidopsis (Long et al., 1996)and OSH1 inrice (Tsuda et al., 2011) have also displayed meristem termination phenotypes.
In recent studies, the discovery of the mechanistic links between the
Page 6 of 45
transcription systems controlling the SAM activity and the hormone biosynthesis and signalling has been reported (Jasinski et al., 2005, Leibfried et al., 2005, Hay et al., 2002 and Sakamoto et al., 2001). Furthermore, CKs are negative regulators of the root meristem activity, which opposes their promotional role in the shoot organogenesis. The encouraging role of CK on the SAM activity has been confirmed by a mutation analysis of the cytokinin receptor genes in plant species (Higuchi et al., 2004 and Nishimura et al., 2004). These processes occurred by the downstream components of the CKsignalling pathway after its perception and signal transduction (Fig. 1). The effects of these components are not always directly through CK but also by interactions with other hormones or transcription factor complexes (Reviewed in Gupta and Rashotte, 2012). Cytokinin also mediates a number of lightregulated processes, including chloroplast differentiation and de-etiolation (Nemhauser and Chory, 2002); in addition, certain CK functions are primarily executed through the control of the cell cycle activities (Roef and Van Onckelen, 2010). The number of cell divisions and exiting cells from the proliferation state in the meristem basal border are regulated by CK. Exogenous CK primarily decreases the elongation of the wild-type roots by reducing the cell expansion and the size of the meristem rather than by dropping the cell division rate (Werner et al., 2003 and Beemster and Baskin, 2000). It has also been reported that transcriptional factors, such as KNOTTED-like homeo box (KNOX), are dependent on the biosynthesis of CK in meristem cells; in addition, an analysis of the KNOX mutants of rice has shown that the expression of the KNOX gene is positively regulated by the action of CK and KNOX genes themselves (Tsuda et al., 2011). The KNOX proteins, which are encoded by the KNOX genes, have been shown to accumulate in the cells around the SAM. This transcription factor is required for the maintenance of SAM and its activity (Sakamoto et al., 2006, Jasinski et al., 2005 and Yanai et al., 2005). It has also been revealed that OSH1 directly attaches to the five KNOX loci in the rice genome, whichincludesOSH1 and OSH15, by the conserved cis-elements. The positive auto-regulation of OSH1 is an essential factor for its expression and the SAM maintenance.
Thus, the preservation of the
indistinctive state mediated by the positive auto-regulation of a KNOX gene is a requisite mechanism of self-maintenance of the SAM (Tsuda et al., 2011). It has been defined that KNOX 1binds to thousands of loci in the maize genome containing 643 genes that are adapted in one or several tissues. KNOX 1 also binds to the cis-elements present in the high confidence KNOX1-bound loci in the maize. KNOX 1 directly regulates the genes participating in hormonal pathways, especially auxin and TFs with the home box (HB), which affects the plant meristem characteristics and function (Bolduc et al., 2012). Several classes of transcription factors have been shown to participate in the SAM development (Table 1) (Kurakawa et al., 2007 and Leibfried et al., 2005). One of the most important traits in rice is the grain
Page 7 of 45
yield per panicle, which is controlled by the DENSE AND ERECT PANICLE1 (DEP1) (Huang et al., 2009), the WEALTHYFARMER’S PANICLE (WFP), Gn1a (Ashikari et al., 2005), ect QTL loci. Among these genes, Gn1a encodes a cytokinin degradation enzyme (OsCKX2). There is a negative correlation between the expression level of OsCKX2 and the grain yield per plant, confirming the positive influence of the CKs on the grain number per plant. A decreased expression of OsCKX2 leads to CK accumulation within the inflorescence meristems and raises the quantity of the reproductive organs, causing an improved grain yield (Ashikari et al., 2005).
2.1.1 Cytokinin signalling transduction in rice Plants use the two-component phosphorelay systems for signal transduction and the aspects of these two-component systems (TCS), which have been suggested in plant responses to the Cytokinin (Reviewed in Hwang et al., 2002 and Schaller, 2000). A simple TCS is composed of a His sensor kinase (HK) and a response regulator (RR). The His kinase autophosphorylates the conserved His remains in response to the environmental stimulus. This particular phosphate group can then be transferred to the conserved Asp remains inside of the receiver domain of the response regulator.
This response
regulator, which is typically a transcription factor, subsequently regulates the downstream signalling in the pathway. Multistep phosphorelay systems are also identified, which use three elements: a hybrid receptor kinase containing the His kinase and receiver domains in a single protein, a phosphotransfer protein that contains His (HPt), and a response regulator (Schaller, 2000 and Reviewed in Swanson et al., 1994). In the multiple phosphorelay, the particular phosphate is transmitted from amino acid to amino acid between proteins in the sequence His-Asp-His-Asp. In Arabidopsis, the RRs are categorised into type-A (primary CK response genes), -B and -C classes, depending on their amino acid sequences and their domain structure (Reviewed in Lomin et al., 2012, Sakai et al., 2001, Sakai et al., 2000, Kiba et al., 1999, Brandstatter and Kieber, 1998, Sakai et al., 1998 and Taniguchi et al., 1998). The type-A ARRs consist of a receptor domain with a short sequence extension at the N- and the C-terminal ends (Ramireddy, 2009). Variable transcription levels of certain type-A ARRs under biotic and abiotic stresses have been reported (Jeon and Kim, 2013, Jeon et al., 2010, Mason et al., 2010, Wohlbach et al., 2008 and Hass et al., 2004). The GARP (or B motif) domain binding sites are located in the promoters of the type-A ARRs. The GARP is B motif homologous in the type-B ARRs, which generally occur in the GARP family of plant transcription factors (Hosoda et al., 2002). The type-B ARRs may bind to these promoters
Page 8 of 45
and operate the transcription (Sakai et al., 2000). As opposed to the type-A ARRs, the expression level of the type-B ARRs is unaffected by CKs, nitrate, or other plant hormones (Hirose et al., 2007, Imamura et al., 1999 and Lohrmann et al., 1999). Several studies have shown that the type-C ARR genes cannot also be activated by CK (Gattolin et al., 2006). Others studies have mentioned that the type-C ARRs may play different roles in the CK-signalling pathway (Horak et al., 2008). The transcription levels of most of the OsRRs genes are quickly enhanced under exogenous CK application in rice (Du et al., 2007). However, the type-B ARRs include a receptor domain and a large C-terminal. In Arabidopsis, three Hissensor kinases involving Arabidopsis Histidine Kinase 2 (AHK2), AHK3 and AHK4 are cytokinin receptors (Inoue et al., 2001, Suzuki et al., 2001, Ueguchi et al., 2001 and Yamada et al., 2001). These CK receivers (AHK2, AHK3 and AHK4) are effective in the shoot and root development, leaf senescence, seed size, germination, and the metabolism of CKs in Arabidopsis and maize (Wang et al., 2014, Reviewed in ElShowk et al., 2013 and Riefler et al., 2006). AHK4 is known as Cytokinin Response 1 (CRE1) or Wooden Leg 1 (WOL1), which is a primary receptor directly bound to a variety of CKs (natural and synthetic) in a significantly specific manner in Arabidopsis. A single amino acid replacement (Thr-301 to Ile) in the extracellular domain of AHK4 results in its incapability to bind to the CKs. This mutation confirmed the transducer role of AHK4 and its two homologues, AHK2 and AHK3, for the CK signals across the plasma membrane (PM) in Arabidopsis. The His-kinase activity of AHK4 is promoted by the direct attachment of CK to the extracellular domain. Thus, AHK4alone distributes these hormonal signals through the membrane (Yamada et al., 2001). Subsequently, the signals are transmitted by the HPs to the RRs in the nucleus, which suppress or activate transcription. Two additional His sensor kinases, Cytokinin Insensitive 1 (CKI1) and AHK1, include a putative ligand binding domain that does not have a significant similarity to the ligand domains of the cytokinin receptors, indicating their particular involvement in the sensing of additional stimuli (Schaller et al., 2008). The TCS pathways are have clearly been suggested as a factor in the plant’s response to cytokinin, which is considered to incorporate all of the components of a multistep phosphorelay system (Hwang and Sheen, 2001). Based on the recommended model, the CK receptors autophosphorylate in response to CK. This phosphate can then be transmitted to an HPt protein, which then travels into the nucleus and triggers the type-B ARRs by transporting the phosphate to them. One of several transcriptional targets of the type-B ARRs is typically the type-A ARRs that upon induction, act as negative modulators of the primary signal transduction pathway (To et al., 2004). To date, the most powerful proof for the function of the type-B ARRs in regulating the CK signal has been derived from the
Page 9 of 45
analysis of ARR1. A null mutation within ARR1 leads to a diminished sensitivity to CK in shoot regeneration and root elongation assays (Sakai et al., 2001). In Arabidopsis, over-expression of ARR1 and ARR2 causes an increased sensitivity to CK (Hwang and Sheen, 2001 and Sakai et al., 2001). There are ten type-A ARRs, which arrange into five similar pairs. The actual transcription rates of most of the type-A ARRs (not the type-B ARRs) are typically quickly and particularly activated in response to the exogenous CK, and this activation occurs in the absence of de novo protein synthesis (D'Agostino et al., 2000 and Taniguchi et al., 1998). The gene expression differs among the various type-A ARRs, with ARR4, ARR8, and ARR9 showing relatively high basal ranges, and ARR5, ARR6, ARR7 and ARR15 displaying the maximum fold induction in response to CK (Rashotte et al., 2003 and D'Agostino et al., 2000). The transcription of the type-A ARRs is regulated simply by the type-B ARRs (Hwang and Sheen, 2001 and Sakai et al., 2001). Over-expression of several type-A ARRs suppresses the expression of the ARR6 promoter-luciferase reporter in the cell culture of Arabidopsis, indicating that the type-A ARRs can adversely regulate their particular transcription (Hwang and Sheen, 2001). The homologs of the type-A ARRs and type-B ARRs are found in various other dicotyledonous and monocotyledonous plants, such as maize (Zea mays L.) and rice (Oryza sativa L.) (Asakura et al., 2003 and Reviewed in Haberer and Kieber, 2002). In rice, two CK-signalling pathways have been suggested; one pathway is mediated by the twocomponent regulatory systems, and the other pathway is mediated using CHARK (CHASE domain Receptor-like serine/threonine Kinase) through serine/threonine phosphorylation (Tsai et al., 2012, Yonekura-Sakakibara et al., 2004 and Reviewed in Hutchison and Kieber, 2002). The CK signalling system in rice, which is the same as that in Arabidopsis, typically includes a sensory histidine kinase (HK), a histidine phosphotransfer protein (HP) and a response regulator (RR) (Fig. 1); however, whether the roles of the rice HPs have diverged remains unclear. In rice plants, five different CK-response histidine protein kinases (HKs) (OsHK1-4, and OsHKL1), fifteen response regulators (type-A OsRRs) (OsRR1-15), seven type-B OsRR genes (OsRR16-22), five pseudo-response regulators (OsPRR1-5) and two Authentic HPs (OsAHP1 and OsAHP2) have been identified (Sun et al., 2014 and Du et al., 2007). The Ehd1, a typeB OsRR with a novel two-component signalling cascade, is integrated in the photoperiodic control pathway of flowering in rice (Du et al., 2007). The OsAHPs phosphorylate the type-A and type-B OsRRs in the nucleus of rice cells. The phosphorylated type-A OsRRs can initiate transcription of the target genes (CYTOKININ RESPONSE FACTOR (CRF) and type-A OsRRs genes). The type-A OsRRs, as negative inhibitors of the CK signalling, receive phosphoryl groups from the OsAHPs. The type-A OsRRs are stabilised by phosphorylation; otherwise, its protein will be degraded. The CRFs mediate the CK
Page 10 of 45
responses accompanied by the His-Asp phosphorelay system (Rashotte et al., 2006) and promote the transcription of the CK response genes. Several targets of the CRFs and the type-B OsRRs are collective, although certain targets are specific to the each of them. In these schemes, the signals are transferred through the phosphoryl groups bound to the histidine and aspartic residues. Membrane-located HK plays a role as a sensor of the CKs. In the second CK-signalling pathway, the transporter domain individually includes a typical sequence motif and a histidine residue and is the location of the auto phosphorylation (Reviewed in West and Stock, 2001). A domain, which is a putative recognition site for CK shared by all of the HKs, was identified during the prediction of the extracytoplasmic regions and the design of cyclase/histidine kinase-associated sensory extracellular (CHASE) domains (Anantharaman and Aravind, 2001, Ueguchi et al., 2001 and Yamada et al., 2001). The CHASE domain is located outside of the PM and binds CK. Binding of CK motivates conformational changes in the proteins, which activate the transfer of a phosphoryl group between the conserved phosphor-admitting His and Asp residues. The OsAHPs (Authentic HPs) are transported through the nuclear membrane (NM) to the nucleus when they are phosphorylated in rice (Sun et al., 2014). AtHK1, a putative osmosensor, has been identified to interact with AtHPt1 (a phosphotransfer protein) in Arabidopsis. A similar interaction has been found between OsHK3b, the ortholog of AtHK1, and OsHPt2 in rice. The presence of a transmitter domain (TD) and a receiver domain (RD) has been confirmed in AtHK1 by analysis of its amino acid sequence, whereasOsHK3b contains three conserved domains known as CHASE, TD and RD. A binding analysis of the RD domain of these sensors in Arabidopsis and rice has confirmed the role of the different residues, such as His in the HPt protein, which is required for their interaction (Kushwaha et al., 2014).
2.1
Auxin signalling in the SAM
Auxins, as with other phytohormones, can control many aspects of plant growth and development. These features are involved in the branching of the shoot and root and in the differentiation of the vascular system (Reviewed in Leyser, 2006 and Reinhardt et al., 2000). Over the past decade, it has been shown that auxin plays roles not only as the primary regulator of organogenesis at the SAM but also as a central determinant of the self-organising characteristics of phyllotaxis (Reviewed in Sassi and Vernoux, 2013 and Reinhardt et al., 2003). Five tryptophan (TRP) auxin biosynthetic pathways have been reported. Four of these pathways are TRP-dependent, including the indole-3-pyruvic acid (IPA), indole-3-acetaldoxime (IAOx), tryptamine (TAM), and indole-3-acetamide (IAM) pathways, and one pathway is TRP-independent in monocots, such as rice (Fig. 3). The IAM is converted to IAA through the action of the amidase genes. These genes have not yet been characterised in monocots, although an
Page 11 of 45
IAM hydrolase activity has been identified in rice callus; therefore, it appears that this pathway is used in grasses (Arai et al., 2004). The IPA pathway is important in the monocot and dicot growth. TRPaminotransferase genes, such as TAR1 and TAA1, convert TRP to IPA in Arabidopsis (Stepanova et al., 2008 and Tao et al., 2008). TAA1-like genes have not yet been identified in rice. It has been suggested that IPA is changed to indole-3-acetaldehyde (IAAId) through the IPA decarboxylase activity; furthermore, IAAId is converted to IAA by an aldehyde oxidase, which is encoded by the OsAO1 gene in rice (Yamamoto et al., 2007). The TAM pathway plays an important role in different developmental stages of monocots and dicots. The auxin biosynthesis is regulated by several gene families. The YUC gene family is involved in auxin biosynthesis and encodes flavin mono oxygenase-like enzymes that are responsible for regulating the TAM pathway.
YUC can convert tryptamine (TAM) to N-
hydroxytryptamine (NHT) in vitro, suggesting that the N-oxygenation of TAM, a rate limiting step in the biosynthesis of auxin in plants, is catalysed by YUC. Among the 13 YUC-like genes identified in rice, only two (OsYUCCA1 and CONSTITUTIVELY WILTED1 (OsCOW1)) have been functionally studied (Woo et al., 2007 and Yamamoto et al., 2007). Over-expression of OsYUCCA1 has shown enhanced IAA levels and has been attributed to the over-production of the auxin phenotypes, whereas plants expressing the antisense OsYUCCA1 cDNA have shown problems that resemble those of the rice auxin-insensitive mutants. These findings have demonstrated the crucial role for the OsYUCCA1 in the IAA biosynthesis through the TRP-dependent pathway. In addition, homozygous plants with the inserted OsCOW1 gene, which encodes a member of the YUCCA family of proteins, have shown decreased leaf widths and root to shoot ratios. Once the oscow1 seedlings have been grown under low intensity light and increased relative humidity, the rolled leaf characteristic is significantly improved. Therefore, these observations have suggested that OsCOW1- mediated IAA biosynthesis has an important role in conserving the root to shoot ratios, thus affecting water homeostasis in rice.
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After the identification of this family, it was demonstrated that this gene family maintains excellent control of the auxin biosynthesis and plays a basic role in the shoot meristem activity (Zhao et al., 2001). The IAOx pathway is believed to be active only in cruciferous species, such as Arabidopsis, but there is contradictory evidence suggesting that this pathway may also occur in monocots (Sugawara et al., 2009). For example, indole-3-acetonitrile (IAN) is converted to IAA by the action of the nitrilase genes in Arabidopsis.
Nitrilase genes have also been identified in maize (ZmNIT2) (Park et al., 2003).
Additionally, genes analogous to ZmNIT2 have been reported but not characterised in rice (Yamamoto et al., 2007). Organ pericarp mutants in maize have also been studied; the mutants show an inability to produce TRP but continued to produce auxin. It has been confirmed that TRP-independent biosynthesis occurs in maize (Wright et al., 1991). When auxin is not produced from TRP, it is thought to be made through indole-3-glycerol phosphate or indole; however, the genes involved in this pathway have not been characterised for monocots or dicots (Reviewed in Woodward and Bartel, 2005). It has been demonstrated that auxin moves between cells along the shoot-root axis in a polar manner with the help of carrier proteins involving influx and efflux carriers (Sieberer and Leyser, 2006) (Table 2), although the regulation and differentiation of the tissue in response to auxin varies locally (Kramer and Bennett, 2006, Weijers et al., 2005, Benkova et al., 2003 and Reinhardt et al., 2003). Moreover, the concentrations of the local auxin are under the control of an active combination of polar auxin transport, auxin synthesis, catabolism, and conjugation in the shoot meristem cells. A gene family of 31 members produces the Auxin/IAA proteins in rice (Jain et al., 2006). These proteins are short-lived transcriptional regulators that mediate theauxin responses accompanied by the F-box protein transport inhibitor response1 (TIR1) protein, an auxin receptor. The OsIAA1/3gene was the first reported AUX/IAA gene in rice. Auxin induces the transcription of OsIAA1/3; however, light suppresses its expression (Nakamura et al., 2006, Thakur et al., 2001). Alternatively, OsIAA1/3 is expressed in nearly all of the plant organs and tissues (Song et al., 2009). OsIAA4 encodes a protein that contains 204 amino acids with four domains. OsIAA4 has the same domain II as AtIAA31, containing a G-to-D substitution. In Arabidopsis, shy2-3, iaa18-1 and AtAA31 include a dominant mutation-type domain II that would result in a dominant mutation of the Aux/IAA genes. Its core amino acid motif is “DWPPV/I”, although the canonical Aux/IAA protein contains a core motif of domain II known as “GWPPV”; therefore, OsIAA4 can
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be considered as a dominant-mutation class of protein in rice. The over-expression of the OsIAA4 gene in rice plants has illustrated dwarfism, enhanced tiller angles, decreased gravity response and less sensitivity to 2,4-dichlorophenoxyacetic acid (2,4-D) (Song and Xu, 2013).
2.1.1 Auxin and the shoot branching pattern (Tillering) in rice A shoot branching pattern is an important factor in plant architecture. This pattern is arranged by the following two independent stages: the formation of axillary lateral buds in the axil of the leaves followed by bud outgrowth. The apical dominance, as a central mechanism, suppresses the axillary bud growth through the apical meristem growth (McSteen and Leyser, 2005). The presence of the SAM affects the suppression of the lateral bud outgrowth, whereas the lateral bud is initiated by the removal of this meristem (Beveridge, 2006). The apically derived auxin suppresses the bud activity, whereas CK promotes it. In rice plants, shoot branching is the result of a developmental hold of the lateral buds produced by the absence of auxin, which is transferred from the SAM. The lateral bud outgrowth might be controlled by the enhanced biosynthesis of a group of inhibitors (Foo et al., 2005). Auxin suppresses the bud outgrowth via at least two different pathways; one pathway requires the branching inhibitor encoded by dwarf10 (d10), whereas the other pathway is self-regulating and is independent of this branching inhibitor. The presence of d10, an ortholog of RAMOSUS1 (RMS1), DECREASED APICAL DOMINANCE1 (DAD1) and MORE AXILLARY BRANCHING4 (MAX4)in rice and encodes the carotenoid cleavage dioxygenases, could be crucial for the regulation of the branching inhibitor pathway (Arite et al., 2007). Tillering is one of the most important components affecting the rice yield, and there is a long history of its study. Tillering is controlled by a two-step process of axillary meristem initiation and dormancy. The axillary meristem initiation is strongly dominated by the LAX PANICLE 1 pathway, whereas dormancy is clearly controlled by auxin and cytokinin in rice (Reviewed in Zhang and Yuan, 2014 and Reviewed in Pautler et al., 2013). Ran (Ras-related nuclear) was identified as a conserved eukaryotic GTPase. The over-expression analysis of Ran1 has shown a stimulating hypersensitivity to the exogenous auxins resulting in an increased number of tillers in transgenic rice plants (Wang et al., 2006). In addition, the phenotypes of OsmiR393-overexpression in rice are caused by the hyposensitivity to the auxin signal due to the decreased expression levels of two auxin receptor genes (RICETRANSPORT INHIBITOR RESPONSE 1 (OsTIR1) and AUXIN SIGNALING F-BOX 2(OsAFB2)), also leading to increased tiller numbers. Subsequently, the over-expression of OsmiR393 suppresses the expression of an auxin transporter
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(OsAUX1) and the tillering inhibitor (RICE TEOSINTE BRANCHED 1(OsTB1)) genes. Finally, a gene chain beginning with OsmiR393 to rice tillering, maybe from OsTIR1 and OsAFB2 to OsAUX1, affects the transportation of auxin, and OsTB1, which resulted in the regulation of tillering (Xia et al., 2012). In the rice genome, the LAXPANICLE (LAX), SMALL PANICLE (SPA) and MONOCULM 1 (MOC1) genes are also responsible for the regulation of the axillary meristem creation and the shoot branching (tiller) (Komatsu et al., 2003). A basic helix-loop-helix transcription factor is encoded by LAX, which is expressed into the boundary of SAM and the region of new meristem growth. LAX is a major factor in the formation of axillary meristems during morphogenesis in rice plants (Komatsu et al., 2003). At least seven homologs of the PIN (PIN-Formed, polar auxin transporter) gene have been characterised in the rice genome (Xu et al., 2005 and Morita and Kyozuka, 2004). Except for OsPIN1, the exact role of the other PIN genes in rice and their function in the regulation of the tiller growth remain unclear and must be determined in future studies (Xu et al., 2005).
2.1.2 Auxin and panicle formation in rice Two meristems, a primary SAM and the root meristem, are the primary axis of organogenesis in plants. The primary SAM generates several axillary meristems that become the panicle branches. The SAM of the panicle branches acts as the primary SAM and continuously produces higher-order axillary meristems.
The primary meristem of a panicle (inflorescence meristem) produces the rachis and the lateral meristems (also called the primary and secondary branching meristems) that will give rise to the primary branch axis. Finally, the lateral buds develop into the branching meristem, the spikelet meristem that differentiates the glumes and, subsequently, the floret meristem (Kurakawa et al., 2007); therefore, the panicles, panicle branches and lateral spikelets are created as axillary meristems in rice plants. From an agronomic viewpoint, the grain yield is normally supplied by the initial tillers and certain early secondary tillers, whereas the tertiary and next secondary tillers contribute only a small portion. In breeding programs, there is an interest in breeding rice plants with fewer and larger panicles to generate high yields (Reviewed in Khush, 2001). Thus, to increase the rice yield, the axillary bud activity should be inhibited in a timely manner via genetic and hormonal manipulation. Tillering and panicle formation share extensive similarities because they both engage with the apical growth and branching. Hence, analogous regulatory mechanisms could contribute to both of the processes.
The final plant
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architecture and panicle size are the products of a balance between the apical dominance and the branching at different levels. Cytokinin has been elucidated as a promoter of branching, resulting in increased spikelet numbers. Auxin provided by the primary shoot apex suppresses the axillary bud growth; however, CK reduces the inhibition and leads to the outgrowth of lateral branches (Taiz and Zeiger, 2006). However, whether auxinplays any role in the panicle size remains to be clarified.
3
Auxin/Cytokinin crosstalk and other hormones in SAM
The function of SAM relies on the combination of several hormones and their interactions (Fig. 4). Recent findings have suggested that the effects of high CK signalling on the stem cell activity are crucial for the preservation of the meristem cells. However, the initiation of certain organ development has been reported using an accurate balance between the divergent effects of CK on auxin (Sablowski, 2011). CK regulates the auxin biosynthesis conversely. The control of the CK-signalling pathway activity by auxin is mediated by the transcriptional modulation of its signal transduction. However, CK has shown feedback to the auxin activity by the conversion of the AUX/IAA genes expression involved in suppressing the auxin signalling pathway. Thus, CK directly affects the auxin diffusion mediated by the PIN family (auxin efflux carriers), whose expression is controlled by the auxin signalling pathway (Ruzicka et al., 2009 and Ioio et al., 2008). Recently, it has been reported that CK affects the adequate apicalbasal gynoecium differential patterning in Arabidopsis in an analogous manner to the suppression of the polar auxin transport, and a relationship between both of the hormones in this process has been suggested (Zuniga-Mayo et al., 2014 and Marhavy et al., 2011). A range of CKs led to enhanced auxin synthesis in young leaves, the shoot apex and the root system. This opposing effect was increased in the CK-hypersensitive-ARR mutant arr3, arr4, arr5, and arr6. Treatment of the CK-insusceptible fourfold AHP mutant ahp1, ahp2, ahp3 and ahp4 caused a decrease in the IAA biosynthesis, signifying that the correlation between the CK signalling and the auxin synthesis cannot be straightforward (Jones et al., 2010). An accumulation of the auxin activates organ initiation; however, auxin reduction surrounding the organs produces inhibitory fields that are assumed sufficient to maintain the plant phyllotaxis pattern.
The intercellular movement of the CK-signalling inhibitor ARABIDOPSIS HISTIDINE
PHOSPHOTRANSFER PROTEIN 6 (AHP6) is generated directly downstream of auxin and is involved in regulating the phyllotactic patterns in Arabidopsis. The AHP6-based fields created patterns of CK signalling in the meristem that involved the robustness of the phyllotaxis through the signal of a temporal sequence on the organ initiation. Finally, it has been suggested that two different hormonebased fields may be essential to achieve temporal precision during the arrangement of repetitive
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structures at the SAM, thus indicating an original mechanism for providing robustness to a dynamic developmental system (Besnard et al., 2014). The activity of CK and auxin directly congregates on the promoters of the ARR7 and ARR15 genes, two negative regulators of the CK signalling, and plays important meristematic roles. However, the expression of ARR7 and ARR15 is induced by CK in the SAM and is negatively affected by auxin, which is to a certain extent, mediated by the AUXIN RESPONSE FACTOR5/MONOPTEROS (MP) transcription factor in Arabidopsis (Reviewed in Zhao et al., 2010 and Leibfried et al., 2005). The CLV3 and CLV1 signals suppress the expression of WUS to a limited region inside of the corpus in Arabidopsis (Khurana et al., 2005). AS1 and AS2 are expressed in the stem cells of the Arabidopsis primordium and have a stimulatory effect (Fig. 4) (Cairney, 2007). The negative relationship between the SHOOT MERISTEMLESS (STM) and these two genes maintain the SAM/primordium boundary (Depuydt et al., 2008). The STM positively regulates IPT7 and negatively regulates GA20 oxidase (the enzymes involved in the CK and gibberellins (GA) biosynthesis) in the organ boundary areas of Arabidopsis (Reviewed in Fambrini and Pugliesi, 2013, Hay et al., 2006 and Ogas et al., 1999). CK promotes the expression of ARR7 and ARR15 via a STM-dependent pathway in Arabidopsis (Fig. 4). The negative regulation of WUS by these genes is crucial for stem cell formation (Reviewed in Fambrini and Pugliesi, 2013 and Leibfried et al., 2005). Auxin also interacts with the GAs, another group of hormones in the SAM; furthermore, auxin can activate the ethylene-dependent responses. Recently, it has been suggested that ethylene plays an important role in limiting the cell division in the Quiescent Centre (QC) of the root (Ortega-Martinez et al., 2007, Stepanova et al., 2007), but it is unclear whether it plays a similar role in limiting cell division in the CZ of the SAM. The additive or synergistic interactions of the auxin and brassinosteroids (BR) affects the dynamic behaviour of the SAM (Vandenbussche et al., 2013 and Belkhadir and Chory, 2006). The activation of the DR5 reporters is a specific response of BR to the auxin, which is diminished by the disruption of the BR signalling in Arabidopsis (Mouchel et al., 2006, Bao et al., 2004 and Nakamura et al., 2003). BR signalling is blocked in the dwarf plants phenotype, which can be recovered artificially; however, the expression of this signal in the epidermis is essential and is sufficient for the plant recovery. The priority of the epidermal cell layers in mediating the BR response asserts the “tensile limited growth” patterns (Kutschera, 2008). Based on this pattern, the total growth of the plants shows an equilibration between the extensibility of the superficial layers and the growth promoting turgor strengths. The possible connections of the layer specific responses have been strengthened by studies that have shown a restricted ability of BR for intercellular movement (Symons and Reid, 2004) and epidermally concentrated patterns of auxin transportation in the SAM (Reinhardt et al., 2003). The GA20- and GA3-oxidases are classes of enzymes that are controlled by the
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concentration of GA, and they are essential for GA biosynthesis. Additionally, GA deactivation is controlled via the GA2- oxidases. These classes of enzymes are produced by a family of genes, some of which are expressed principally in the SAM of Arabidopsis.
The beginning of the GA2-oxidases
biosynthesis occurs at the central meristem and is limited to the young organs; however, the enzymes involved in the deactivation of GA are expressed in the base of SAM (Hu et al., 2008, Rieu et al., 2008 and Jasinski et al., 2005). In the seedling stage of Arabidopsis, under auxin treatment, the expression of the GA oxidases by activating or deactivating roles has been confirmed. Among the GA oxidases, at least GA20ox1, GA20ox2, and GA20ox4 are expressed in the SAM; consequently, they could be targets of auxin signalling in the SAM (Frigerio et al., 2006). These GA oxidases have been encoded by the SemiDwarf-1(SD1) gene in rice (Ashikari et al., 2002). A wide range of genes, such as OsMADS1, plays important roles in modulating the expression of the shoot meristem, auxin and CK-mediated signalling events in rice; in addition, a combination of genes are regulated by OsMADS1 involved in developing the rice panicles. The suppression of OsMADS34, a LOFSEP gene, and the induction of the OsMADS55 expression, the identical gene involved in the SHORT VEGETATIVE PHASE-like floret meristem, confirmed its important role in the simplification of the spikelet to floret meristem transition. OsMADS1 is also involved in the direct regulation of transcription factor genes, such as OsHB4 (a homeo domain Leu zipper member), OsBLH1 (a BEL-like homeodomain member), OsKANAD12, OsKANAD14 and OsETTIN2, which illustrates its function in meristem maintenance, determinacy and lateral organ initiation and development. Overall, OsMADS1 has been shown to function in balancing the meristem growth, the lateral organ differentiation and determinacy by promoting the auxin transport, signalling, and auxin reliant expression and its direct suppression of three CK type-A OsRRs (Khanday et al., 2013). Moreover, the interaction of CK-auxin is included in the predominant shoot apex growth, which hinders the axillary bud outgrowth. FON2 and FON4, orthologs of CLV3, encode a secreted protein containing a CLE domain, which is localised at the SAM in rice plants. The function of FON2 and FON4 depends on the action of the FON1, ortholog of CLV1 (Chu et al., 2006 and Suzaki et al., 2006). The Log gene creates a region with high levels of CK/GA in the CZ of the SAM in rice.
Furthermore, the activation of the organ initiation by auxin as a mobile signal in meristem tissues has been established in the past decade (Braun et al., 2008); however, the characteristics of auxin transportation and its incorporation into the auxin biosynthesis and other hormone signalling during the organisation of cell activation and differentiation remain undiscovered and a challenge for the future.
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4
Conclusion
Various factors, including hormones, govern the remaining pluripotent SAM cells and lead to the formation of the different organs. The interaction of CK and auxin involved in the plant growth and organ formation has been widely considered. The critical roles of CK and auxin in the cell proliferation and new organ creation have been known for a long time. The cell destiny in particular tissues, which can be differentiated to a new shoot or root, is controlled by the ratio between these two hormones. Auxins have been known for their significant roles in establishing the leaf primordia and vascular elements; however, it appears that GAs and BR have a smaller effect on the differentiation pattern of the SAM compared with the other factors. Normal SAM can be formed without a significant activity of these hormones; however, it appears that these hormones are responsible for organogenesis and the maintenance of the SAM cells. Alternatively, understanding the interactions between auxin and CK is essential for controlling the developmental processes, such as the formation and maintenance of SAM, which are key factors for establishing the entire plant body. In the SAM, the CKs promote the proliferation of the stem cells and suppress the stem cell differentiation, whereas auxin plays a role in organ primordium initiation via the inhibition of the CK biosynthesis. Over the past decade, the studies on the hormones, their function and signalling in the plants have primarily focused on an analysis of the mutants of the genes involved in their synthesis, the signalling component, their transportation and the encoding receptors. Although studies have been performed on the different functions and aspects of the gene family members, an understanding of the feedback regulation of the CK and auxin pathways remains complicated. To completely understand the mechanism of CK, auxin and SAM signalling, it is essential to examine the involved genes of the monocotyledons and to evaluate the results by a comparison with dicotyledonous plants, such as Arabidopsis. In the future, it will be interesting not only to identify the genes in the biosynthetic pathway but also to study their function and understand the reason for the multiple pathways for auxin and CK biosynthesis. Furthermore, an investigation into whether there are any changes in the CK and auxin biosynthesis signalling pathways of the meristem cells in response to different conditions will be of interest.
5
Acknowledgements
The authors wish to acknowledge the Long-Term Research Grant Scheme (LRGS), Food Security project, Ministry of Higher Education, Malaysia, for the financial support.
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6
References
Anantharaman, V. and Aravind, L., 2001. The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci. 26, 579582. Arai, Y., Kawaguchi, M., Syono, K. and Ikuta, A., 2004. Partial purification of an enzyme hydrolyzing indole-3-acetamide from rice cells. J Plant Res. 117, 191-198. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H. and Kyozuka, J., 2007. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51, 1019-1029. Asakura, Y., Hagino, T., Ohta, Y., Aoki, K., Yonekura-Sakakibara, K., Deji, A., Yamaya, T., Sugiyama, T. and Sakakibara, H., 2003. Molecular characterization of His-Asp phosphorelay signaling factors in maize leaves: implications of the signal divergence by cytokinin-inducible response regulators in the cytosol and the nuclei. Plant Mol Biol. 52, 331-341. Ashikari, M., Sasaki, A., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Datta, S., Ishiyama, K., Saito, T., Kobayashi, M. and Khush, G.S., 2002. Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice 'green revolution'. Breed Sci. 52, 143-150. Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H. and Matsuoka, M., 2005. Cytokinin oxidase regulates rice grain production. Science. 309, 741-745. Attia, K.A., Abdelkhalik, A.F., Ammar, M.H., Wei, C., Yang, J., Lightfoot, D.A., El-Sayed, W.M. and ElShemy, H.A., 2009. Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice. Curr Iss Mol Biol. 11, I29.
Page 20 of 45
Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T. and Yang, Z., 2004. Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134, 1624-1631. Beemster, G.T.S. and Baskin, T.I., 2000. STUNTED PLANT 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol. 124, 1718-1727. Belkhadir, Y. and Chory, J., 2006. Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science. 314, 1410-1411. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G. and Friml, J., 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 115, 591–602. Besnard, F., Refahi, Y., Morin, V., Marteaux, B., Brunoud, G., Chambrier, P., Rozier, F., Mirabet, V., Legrand, J. and Laine, S., 2014. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature. 505, 417-424. Beveridge, C.A., 2006. Axillary bud outgrowth: sending a message. Curr Opin Plant Biol. 9, 35-40. Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O'Connor, D., Grotewold, E. and Hake, S., 2012. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26, 16851690. Brandstatter, I. and Kieber, J.J., 1998. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell. 10, 1009-1019. Braun, N., Wyrzykowska, J., Muller, P., David, K., Couch, D., Perrot-Rechenmann, C. and Fleming, A.J., 2008. Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell
Page 21 of 45
division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell. 20, 2746–2762. Capron, A., Chatfield, S., Provart, N. and Berleth, T., 2009. Embryogenesis: pattern formation from a single cell. The Arabidopsis Book/American Society of Plant Biologists 7. Cho, S.-H., Yoo, S.-C., Zhang, H., Lim, J.-H. and Paek, N.-C., 2014. Rice NARROW LEAF1 Regulates Leaf and Adventitious Root Development. Plant Mol Biol Rep. 32, 270-281. Chu, H., Qian, Q., Liang, W., Yin, C., Tan, H., Yao, X., Yuan, Z., Yang, J., Huang, H. and Luo, D., 2006. The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant physiol. 142, 1039-1052. D'Agostino, I.B., Deruere, J. and Kieber, J.J., 2000. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124, 1706-1717. Depuydt, S., Dolezal, K., Van Lijsebettens, M., Moritz, T., Holsters, M. and Vereecke, D., 2008. Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol. 146, 1267-1281. Dievart, A., Coudert, Y., Gantet, P., Pauluzzi, G., Puig, J., Fanchon, D., Ahmadi, N., Courtois, B., Guiderdoni, E. and Perin, C., 2013. Dissecting the biological bases of traits of interest in rice: Architecture and development of the root system. Cah Agric. 22, 475-483. Du, L., Jiao, F., Chu, J., Jin, G., Chen, M. and Wu, P., 2007. The two-component signal system in rice (Oryza sativa L.): A genome-wide study of cytokinin signal perception and transduction. Genomics. 89, 697-707.
Page 22 of 45
El-Showk, S., Ruonala, R. and Helariutta, Y., 2013. Crossing paths: cytokinin signalling and crosstalk. Development. 140, 1373-1383. Fambrini, M. and Pugliesi, C., 2013. Usual and unusual development of the dicot leaf: involvement of transcription factors and hormones. Plant Cell Rep. 1-24. Foo, E., Bullier, E., Goussot, M., Foucher, F., Rameau, C. and Beveridge, C.A., 2005. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell. 17, 464474. Frigerio, M., Alabadi, D., Perez-Gomez, J., Garcia-Carcel, L., Phillips, A.L., Hedden, P. and Blazquez, M.A., 2006. Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142, 553–563. Friml, J., 2003. Auxin transport—shaping the plant. Curr Opin Plant Biol. 6, 7–12. Fujino, K., Matsuda, Y., Ozawa, K., Nishimura, T., Koshiba, T., Fraaije, M.W. and Sekiguchi, H., 2008. NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genomics. 279, 499507. Gattolin, S., Alandete-Saez, M., Elliott, K., Gonzalez-Carranza, Z., Naomab, E., Powell, C. and Roberts, J.A., 2006. Spatial and temporal expression of the response regulators ARR22 and ARR24 in Arabidopsis thaliana. J Exp Bot. 57, 4225-4233. Giulini, A., Wang, J. and Jackson, D., 2004. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature. 430, 1031-1034. Gupta, S. and Rashotte, A.M., 2012. Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep. 31, 801-812.
Page 23 of 45
Haberer, G. and Kieber, J.J., 2002. Cytokinins. New insights into a classic phytohormone. Plant Physiol. 128, 354-362. Hass, C., Lohrmann, J., Albrecht, V.n., Sweere, U., Hummel, F., Yoo, S.D., Hwang, I., Zhu, T., Schufer, E. and Kudla, J.r., 2004. The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J. 23, 3290-3302. Hay, A., Kaur, H., Phillips, A., Hedden, P., Hake, S. and Tsiantis, M., 2002. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol. 12, 1557-1565. Hay, A., Barkoulas, M. and Tsiantis, M., 2006. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development. 133, 3955-3961. Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A. and Meyerowitz, E.M., 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 15, 1899-1911. Higuchi, M., Pischke, M., nen, A.M.h., Miyawaki, K., Hashimoto, Y., Seki, M., Kobayashi, M., Shinozaki, K., Kato, T. and Tabata, S., 2004. In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci U S A. 101, 8821-8826. Hirano, K., Aya, K., Hobo, T., Sakakibara, H., Kojima, M., Shim, R.A., Hasegawa, Y., Ueguchi-Tanaka, M. and Matsuoka, M., 2008. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol. 49, 1429-1450.
Page 24 of 45
Hirose, N., Makita, N., Kojima, M., Kamada-Nobusada, T. and Sakakibara, H., 2007. Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol. 48, 523-539. Horak, J., Grefen, C., Berendzen, K., Hahn, A., Stierhof, Y.-D., Stadelhofer, B., Stahl, M., Koncz, C. and Harter, K., 2008. The Arabidopsis thaliana response regulator ARR22 is a putative AHP phosphohistidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol. 8, 77. Hosoda, K., Imamura, A., Katoh, E., Hatta, T., Tachiki, M., Yamada, H., Mizuno, T. and Yamazaki, T., 2002. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell. 14, 2015-2029. Hu, J., Mitchum, M.G., Barnaby, N., Ayele, B.T., Ogawa, M., Nam, E., Lai, W.-C., Hanada, A., Alonso, J.M. and Ecker, J.R., 2008. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell. 20, 320-336. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J. and Fu, X., 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet. 41, 494-497. Hutchison, C.E. and Kieber, J.J., 2002. Cytokinin signaling in Arabidopsis. Plant Cell. 14, S47-S59. Hwang, I., Chen, H.-C. and Sheen, J., 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 129, 500-515. Hwang, I. and Sheen, J., 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature. 413, 383-389.
Page 25 of 45
Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Kiba, T., Ueguchi, C., Sugiyama, T. and Mizuno, T., 1999. Compilation and characterization of Arabiopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40, 733-742. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K. and Kakimoto, T., 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 409, 1060-1063. Ioio, R.D., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M.T., Aoyama, T., Costantino, P. and Sabatini, S., 2008. A genetic framework for the control of cell division and differentiation in the root meristem. Science. 322, 1380-1384. Ito, Y. and Kurata, N., 2006. Identification and characterization of cytokinin-signalling gene families in rice. Gene. 382, 57-65. Itoh, J.-I., Kitano, H., Matsuoka, M. and Nagato, Y., 2000. SHOOT ORGANIZATION genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell. 12, 2161-2174. Itoh, J.-I., Nonomura, K.-I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H. and Nagato, Y., 2005. Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46, 23-47. Jain, M., Kaur, N., Garg, R., Thakur, J.K., Tyagi, A.K. and Khurana, J.P., 2006. Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa L.). Funct Integr Genomics.. 6, 47-59. Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P. and Tsiantis, M., 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol. 15, 1560-1565.
Page 26 of 45
Jeon, J. and Kim, J., 2013. Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant physiol. 161 408–424 Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novak, O., Ku, S.-J., Cho, C., Lee, D.J., Lee, E.-J. and Strnad, M., 2010. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem. 285, 23371-23386. Jin, J., Huang, W., Gao, J.-P., Yang, J., Shi, M., Zhu, M.-Z., Luo, D. and Lin, H.-X., 2008. Genetic control of rice plant architecture under domestication. Nat genet. 40, 1365-1369. Jones, B., Gunneras, S.A., Petersson, S.V., Tarkowski, P., Graham, N., May, S., Dolezal, K., Sandberg, G. and Ljung, K., 2010. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell. 22, 2956-2969. Kawakatsu, T., Taramino, G., Itoh, J.I., Allen, J., Sato, Y., Hong, S.K., Yule, R., Nagasawa, N., Kojima, M. and Kusaba, M., 2009. PLASTOCHRON3/GOLIATH encodes a glutamate carboxypeptidase required for proper development in rice. Plant J. 58, 1028-1040. Kerstetter, R.A. and Hake, S., 1997. Shoot meristem formation in vegetative development. Plant Cell. 9, 1001. Khanday, I., Yadav, S.R. and Vijayraghavan, U., 2013. Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol. 161, 1970-1983. Khurana, J.P., Tripathi, L., Kumar, D., Thakur, J.K. and Malik, M.R., 2005. Cell Differentiation in Shoot Meristem: A Molecular Perspective, Plant biotechnology and molecular markers. Springer, pp. 366-385.
Page 27 of 45
Khush, G.S., 2001. Green revolution: the way forward. Nat Rev Genet. 2, 815-822. Kiba, T., Taniguchi, M., Imamura, A., Ueguchi, C., Mizuno, T. and Sugiyama, T.,1999. Differential expression of genes for response regulators in response to cytokinins and nitrate in Arabidopsis thaliana. Plant Cell Physiol. 40, 767-771. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G. and Hwang, I., 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci U S A. 103, 814-819. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K. and Kyozuka, J., 2003. LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci. 100, 1176511770. Kramer, E.M. and Bennett, M., 2006. Auxin transport: a field in flux. Trends Plant Sci. 11, 382–386. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., Sakakibara, H. and Kyozuka, J., 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 445, 652-655. Kushwaha, H.R., Singla-Pareek, S.L. and Pareek, A., 2014. Putative osmosensor-OsHK3b-a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J Biomol Struct Dyn. 32, 1318-1332. Kutschera, U., 2008. The pacemaker of plant growth. Trends Plant Sci. 13, 105-107. Laplaze, L., Benkova, E., Casimiro, I., Maes, L., Vanneste, S., Swarup, R., Weijers, D., Calvo, V., Parizot, B. and Herrera-Rodriguez, M.B.a., 2007. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell. 19, 3889-3900.
Page 28 of 45
Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J. and Lohmann, J.U., 2005. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature. 438, 1172-1175. Leyser, O., 2006. Dynamic integration of auxin transport and signaling. Curr Biol. 16, 424–433. Li, P., Wang, Y., Qian, Q., Fu, Z., Wang, M., Zeng, D., Li, B., Wang, X. and Li, J., 2007. LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Res. 17, 402-410. Lohrmann, J., Buchholz, G., Keitel, C., Sweere, U., Kircher, S., Baurle, I., Kudla, J., Schufer, E. and Harter, K., 1999. Differential Expression and Nuclear Localization of Response Regulator-Like Proteins from Arabidopsis thaliana1. Plant Biol. 1, 495-505. Lomin, S.N., Krivosheev, D.M., Steklov, M.Y., Osolodkin, D.I. and Romanov, G.A., 2012. Receptor properties and features of cytokinin signaling. Acta Naturae. 4, 31. Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K., 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature. 379, 66-69. Marhavy, P., Bielach, A., Abas, L., Abuzeineh, A., Duclercq, J., Tanaka, H., Parezova, M., Petrasek, J., Friml, J. and Kleine-Vehn, J., 2011. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell. 21, 796-804. Mason, M.G., Jha, D., Salt, D.E., Tester, M., Hill, K., Kieber, J.J. and Eric Schaller, G., 2010. Type-B response regulators and ARR12 regulate expression of AtHKT1; 1 and accumulation of sodium in Arabidopsis ARR1 shoots. Plant J. 64, 753-763. McSteen, P. and Leyser, O., 2005. Shoot branching. Annu. Rev. Plant Biol. 56, 353-374. Morita, Y. and Kyozuka, J., 2004. Identification of rice PIN homologs. Rice Genet Newsl. 21, 87-88.
Page 29 of 45
Morita, Y. and Kyozuka, J., 2007. Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. Plant Cell Physiol. 48, 540-549. Mouchel, C.l.F., Osmont, K.S. and Hardtke, C.S., 2006. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature. 443, 458-461. Murray, J.A.H., Jones, A., Godin, C. and Traas, J., 2012. Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell. 24, 3907-3919. Nakamura, A., Higuchi, K., Goda, H., Fujiwara, M.T., Sawa, S., Koshiba, T., Shimada, Y. and Yoshida, S., 2003. Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol. 133, 1843-1853. Nakamura, A., Umemura, I., Gomi, K., Hasegawa, Y., Kitano, H., Sazuka, T. and Matsuoka, M., 2006. Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. Plant J. 46, 297-306. Nemhauser, J. and Chory, J., 2002. Photomorphogenesis. The Arabidopsis Book/American Society of Plant Biologists. 1. Nieminen, K., Immanen, J., Laxell, M., Kauppinen, L., PTarkowski, Dolezal, K., htiharju, S.T., Elo, A., Decourteix, M. and Ljung, K., 2008. Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA. 105, 20032-20037. Nishimura, C., Ohashi, Y., Sato, S., Kato, T., Tabata, S. and Ueguchi, C., 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16, 1365-1377.
Page 30 of 45
Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C., 1999. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Nat Acad Sci. 96, 13839-13844. Ortega-Martinez, O., Pernas, M., Carol, R.J. and Dolan, L., 2007. Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science. 317, 507-510. Park, W.J., Kriechbaumer, V., Muller, A., Piotrowski, M., Meeley, R.B., Gierl, A. and Glawischnig, E., 2003. The nitrilase ZmNIT2 converts indole-3-acetonitrile to indole-3-acetic acid. Plant Physiol. 133, 794-802. Pautler, M., Tanaka, W., Hirano, H.-Y. and Jackson, D., 2013. Grass meristems I: shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant Cell Physiol. 54, 302312. Qi, J., Qian, Q., Bu, Q., Li, S., Chen, Q., Sun, J., Liang, W., Zhou, Y., Chu, C. and Li, X., 2008. Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol. 147, 1947-1959. Ramireddy, E., 2009. Functional characterization of B-type response regulators of Arabidopsis thaliana. Dissertation, Freie Universitat Berlin, Berlin. Rashotte, A.M., Carson, S.D.B., To, J.P.C. and Kieber, J.J., 2003. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 132, 1998-2011. Rashotte, A.M., Mason, M.G., Hutchison, C.E., Ferreira, F.J., Schaller, G.E. and Kieber, J.J., 2006. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a twocomponent pathway. Proc Natl Acad Sci. 103, 11081-11085.
Page 31 of 45
Reinhardt, D., Mandel, T. and Kuhlemeier, C., 2000. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell. 12, 507–519. Reinhardt, D., Pesce, E., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C., 2003. Regulation of phyllotaxis by polar auxin transport. Nature. 426, 255–260. Riefler, M., Novak, O., Strnad, M. and lling, T.S., 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell. 18, 40-54. Rieu, I., Eriksson, S., Powers, S.J., Gong, F., Griffiths, J., Woolley, L., Benlloch, R., Nilsson, O., Thomas, S.G. and Hedden, P., 2008. Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell. 20, 2420-2436. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H., 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science. 283, 1541-1544. Roef, L. and Van Onckelen, H., 2010. Cytokinin regulation of the cell division cycle, Plant Hormones. Springer, pp. 241-261. Ruzicka, K., Simaskova, M., Duclercq, J., Petrasek, J., Zazimalova, E., Simon, S., Friml, J., Van Montagu, M.C.E. and Benkova, E., 2009. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci. 106, 4284-4289. Sablowski, R., 2011. Plant stem cell niches: from signalling to execution. Curr Opin Plant Biol. 14, 4-9. Sakai, H., Aoyama, T., Bono, H. and Oka, A., 1998. Two-component response regulators from Arabidopsis thaliana contain a putative DNA-binding motif. Plant Cell Physiol. 39, 1232-1239.
Page 32 of 45
Sakai, H., Aoyama, T. and Oka, A., 2000. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703-711. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S. and Oka, A., 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science. 294, 1519-1521. Sakakibara, H., 2006. Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol. 57, 431449. Sakakibara, H., Takei, K. and Hirose, N., 2006. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 11, 440-448. Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S. and Matsuoka, M., 2001. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 15, 581-590. Sakamoto, T., Sakakibara, H., Kojima, M., Yamamoto, Y., Nagasaki, H., Inukai, Y., Sato, Y. and Matsuoka, M., 2006. Ectopic expression of KNOTTED1- like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol Comm. 142, 54-62. Sassi, M. and Vernoux, T., 2013. Auxin and self-organization at the shoot apical meristem. J Exp Bot. 64, 2579-2592. Schaller, G.E., 2000. Histidine kinases and the role of two-component systems in plants. Adv Bot Res. 32, 109–148. Schaller, G.E., Kieber, J.J. and Shiu, S.-H., 2008. Two-component signaling elements and histidyl-aspartyl phosphorelays. The Arabidopsis Book/American Society of Plant Biologists. 6.
Page 33 of 45
Sieberer, T. and Leyser, O., 2006. Plant science: auxin transport, but in which direction? Science. 312, 858–860. Skoog, F. and Miller, C., 1957. Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol. 11, 118-131. Song, Y., Wang, L. and Xiong, L., 2009. Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta. 229, 577-591. Song, Y. and Xu, Z.-F., 2013. Ectopic overexpression of an AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) gene OsIAA4 in rice induces morphological changes and reduces responsiveness to auxin. Int J Mol Sci. 14, 13645-13656. Srivastava, L.M., 2002. Plant growth and development: hormones and environment, Access Online via Elsevier. Steeves, T.A. and Sussex, I.M., 1989. Patterns in plant development. Cambridge University Press. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.-Y., Dolezal, K., Schlereth, A., Jurgens, G. and Alonso, J.M., 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 133, 177-191. Stepanova, A.N., Yun, J., Likhacheva, A.V. and Alonso, J.M., 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 19, 2169-2185. Sticklen, M.B. and Oraby, H.F., 2005. Invited review: shoot apical meristem: A Sustainable explant for genetic transformation of cereal crops. In Vitro Cell Dev Biol Plant. 41, 187–200.
Page 34 of 45
Su, Y.-H., Liu, Y.-B. and Zhang, X.-S., 2011. Auxin-cytokinin interaction regulates meristem development. Mol Plant. 4, 616-625. Sugawara, S., Hishiyama, S., Jikumaru, Y., Hanada, A., Nishimura, T., Koshiba, T., Zhao, Y., Kamiya, Y. and Kasahara, H., 2009. Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Nat Acad Sci. 106, 5430-5435. Sun, L., Zhang, Q., Wu, J., Zhang, L., Jiao, X., Zhang, S., Zhang, Z., Sun, D., Lu, T. and Sun, Y., 2014. Two Rice Authentic Histidine Phosphotransfer Proteins, OsAHP1 and OsAHP2, Mediate Cytokinin Signaling and Stress Responses in Rice. Plant Physiol. 165, 335-345. Suzaki, T., Toriba, T., Fujimoto, M., Tsutsumi, N., Kitano, H. and Hirano, H.-Y., 2006. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47, 1591-1602. Suzuki, T., Miwa, K., Ishikawa, K., Yamada, H., Aiba, H. and Mizuno, T., 2001. The Arabidopsis sensor Hiskinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42, 107-113. Swanson, R.V., Alex, L.A. and Simon, M.I., 1994. Histidine and aspartate phosphorylation: twocomponent systems and the limits of homology. Trends biochem sci. 19, 485-490. Symons, G.M. and Reid, J.B., 2004. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 21962206. Taiz, L. and Zeiger, E., 2006. Plant Physiology. 4th ed. Sinauer, Sunderland, MA. Tan, L., Li, X., Liu, F., Sun, X., Li, C., Zhu, Z., Fu, Y., Cai, H., Wang, X. and Xie, D., 2008. Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet. 40, 1360-1364.
Page 35 of 45
Tanaka, M., Takei, K., Kojima, M., Sakakibara, H. and Mori, H., 2006. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 45, 1028-1036. Taniguchi, M., Kiba, T., Sakakibara, H., Ueguchi, C., Mizuno, T. and Sugiyama, T., 1998. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429, 259-262. Tao, Y., Ferrer, J.-L., Ljung, K., Pojer, F., Hong, F., Long, J.A., Li, L., Moreno, J.E., Bowman, M.E. and Ivans, L.J., 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 133, 164-176. Thakur, J.K., Tyagi, A.K. and Khurana, J.P., 2001. OsIAA1, an Aux/IAA cDNA from rice, and changes in its expression as influenced by auxin and light. DNA Res. 8, 193-203. To, J.P., Haberer, G., Ferreira, F.J., Deruère, J., Mason, M.G., Schaller, G.E., Alonso, J.M., Ecker, J.R. and Kieber, J.J., 2004. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell. 16, 658-671. To, J.P.C. and Kieber, J.J., 2008. Cytokinin signaling: two-components and more. Trends Plant Sci. 13, 8592. Tsai, Y.-C., Weir, N.R., Hill, K., Zhang, W., Kim, H.J., Shiu, S.-H., Schaller, G.E. and Kieber, J.J., 2012. Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol. 158, 1666-1684. Tsuda, K., Ito, Y., Sato, Y. and Kurata, N., 2011. Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell. 23, 4368-4381.
Page 36 of 45
Ueguchi, C., Koizumi, H., Suzuki, T. and Mizuno, T., 2001. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42, 231-235. Vandenbussche, F., Callebert, P., Zadnikova, P., Benkova, E. and Van Der Straeten, D., 2013. Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. Am J Bot. 100, 215-225. Vernoux, T., Besnard, F. and Traas, J., 2010. Auxin at the Shoot Apical Meristem. Cold Spring Harb Perspect Biol. 2, 1-14. Vollbrecht, E., Reiser, L. and Hake, S., 2000. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development. 127, 3161-3172. Waller, F., Furuya, M. and Nick, P., 2002. OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol Biol. 50, 415-425. Wang, B., Chen, Y., Guo, B., Kabir, M.R., Yao, Y., Peng, H., Xie, C., Zhang, Y., Sun, Q. and Ni, Z., 2014. Expression and functional analysis of genes encoding cytokinin receptor-like histidine kinase in maize (Zea mays L.). Mol Genet Genomics. 1-12. Wang, X., Xu, Y., Han, Y., Bao, S., Du, J., Yuan, M., Xu, Z. and Chong, K., 2006. Overexpression of RAN1 in rice and Arabidopsis alters primordial meristem, mitotic progress, and sensitivity to auxin. Plant Physiol. 140, 91-101. Weijers, D., Sauer, M., Meurette, O., Friml, J., Ljung, K., Sandberg, G., Hooykaas, P. and Offringa, R., 2005. Maintenance of embryonic auxin distribution for apical–basal patterning by PIN-FORMEDdependent auxin transport in Arabidopsis. Plant Cell. 17, 2517–2526.
Page 37 of 45
Werner, T., Motyka, V., Laucou, V., Smets, R., Onckelen, H.V. and lling, T.S., 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 15, 2532-2550. West, A.H. and Stock, A.M., 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci. 26, 369-376. Wohlbach, D.J., Quirino, B.F. and Sussman, M.R., 2008. Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell. 20, 1101-1117. Woo, Y.-M., Park, H.-J., Suudi, M., Yang, J.-I., Park, J.-J., Back, K., Park, Y.-M. and An, G., 2007. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Mol Biol. 65, 125-136. Woodward, A.W. and Bartel, B., 2005. Auxin: regulation, action, and interaction. Ann Bot. 95, 707-735. Wright, A.D., Sampson, M.B., Neuffer, M.G., Michalczuk, L., Slovin, J.P. and Cohen, J.D., 1991. Indole-3acetic acid biosynthesis in the mutant maize orange pericarp, a tryptophan auxotroph. Science. 254, 998-1000. Xia, K., Wang, R., Ou, X., Fang, Z., Tian, C., Duan, J., Wang, Y. and Zhang, M., 2012. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PloS one. 7, e30039. Xu, M., Zhu, L., Shou, H. and Ping, W., 2005. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674–1681.
Page 38 of 45
Xu, Y., Zhang, S., Guo, H., Wang, S., Xu, L., Li, C., Qian, Q., Chen, F., Geisler, M. and Qi, Y., 2014. OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa. L). Plant J. 79, 106-117. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T. and Mizuno, T., 2001. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M. and Sazuka, T., 2007. Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol. 143, 1362-1371. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A. and Ori, N., 2005. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol. 15, 1566-1571. Yonekura-Sakakibara, K., Kojima, M., Yamaya, T. and Sakakibara, H., 2004. Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol. 134, 1654-1661. Yoshikawa, T., Ito, M., Sumikura, T., Nakayama, A., Nishimura, T., Kitano, H., Yamaguchi, I., Koshiba, T., Hibara, K.-I. and Nagato, Y., 2014. The rice FISH BONE gene encodes a tryptophan aminotransferase, which affects pleiotropic auxin-related processes. Plant J. Zadnikova, P. and Simon, R., 2014. How boundaries control plant development. Curr Opin Plant Biol. 17, 116-125. Zhang, D. and Yuan, Z., 2014. Molecular control of grass inflorescence development. Annu Rev Plant Biol. 65, 553-578.
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Zhao, Y., 2008. The role of local biosynthesis of auxin and cytokinin in plant development. Curr Opin Plant Biol. 11, 16-22. Zhao, Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D. and Chory, J., 2001. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science. 291, 306–309. Zhao, Z., Andersen, S.U., Ljung, K., Dolezal, K., Miotk, A., Schultheiss, S.J. and Lohmann, J.U., 2010. Hormonal control of the shoot stem-cell niche. Nature. 465, 1089-1092. Zhuang, X., Jiang, J., Li, J., Ma, Q., Xu, Y., Xue, Y., Xu, Z. and Chong, K., 2006. Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J. 48, 581-591. Zuniga-Mayo, V.M., Reyes-Olalde, J.I., Marsch-Martinez, N. and De Folter, S., 2014. Cytokinin treatments affect the apical-basal patterning of the Arabidopsis gynoecium and resemble the effects of polar auxin transport inhibition. Front Plant Sci. 5. Fig. 1 - Cytokinin signalling in rice. PM: Plasma membrane; NM: Nucleus membrane. The CHASE domain is positioned outside of the PM and binds CK (shown in red). The phosphoryl group is shown in the green circle. His and Asp are shown as H and D, respectively. The OsAHPs are shown with the green rectangle; modified from (El-Showk et al., 2013 and To and Kieber, 2008).
Fig. 2 - A schematic illustration of the cytokinin biosynthesis and activation pathways.Adenosine phosphate-isopentenyl-transferase (IPT) (1); CYP735A (2); Phosphatase (3); 5/- ribonucleotidephosphohydrolase (4); adenosine nucleosidase (5); Zeatinreductase (6); Purine nucleoside phosphorylase (7) Phosphorylation by
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Genes
Functions
References
adenosine kinase (8); modified from (Kurakawa et al., 2007, Sakakibara et al., 2006 and Sakamoto et al., 2006). Fig. 3 - Proposed tryptophan-dependent pathway of IAA biosynthesis in rice.The dotted arrows show the steps that are joined with the glucosinolate pathway. Modified from (Hirano et al., 2008 and Yamamoto et al., 2007)
Fig. 4 - A schematic molecular representation of the Auxin, CK, and Gibberellin (GA) interaction mechanisms in the regulation of meristem development in Arabidopsis (A) Modified from (Su et al., 2011) and rice (B).
Table 1- List of certain cytokinin signalling regulators
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WUSCHEL
Preserves undifferentiated stem cells and directly suppresses
(WUS)
a subgroup of the A form of the ARR genes; also act as a
(Leibfried et al., 2005)
regulator of the cytokinin signal in the negative response manner in Arabidopsis. This gene is homologous to OsWUS in rice. CKX
Reduces the cambial activity as a cytokinin signalling gene in
(Nieminen et al., 2008)
rice, maize and Arabidopsis IPT
Effective for the cambial growth and restricts the import of
(Tanaka et al., 2006)
cytokinins into the axillary bud in rice CHARK
Cytokinin receptor in rice
(Ito and Kurata, 2006)
OsARR2
Mediates a cytokinin signal, most likely through its NH2- (Dievart et al., 2013, Kim et al., terminal signal receiver domain, and transactivates ARR6, which is immediately responsive to the cytokinins.
2006 and Riefler et al., 2006)
Its
orthologous gene reduces the effects of AHK2, and AHK3 and mediates the leaf senescence activity in Arabidopsis OsHK2, 3, 4, 5 OsMADS1
Cytokinin receptor in rice Direct repression of three cytokinin A-type response
(Ito and Kurata, 2006) (Khanday et al., 2013)
regulators and regulates the meristem growth and the lateral organ development in rice OsARR6
A small panicle has been reported in transgenic rice plants
(Hirose et al., 2007)
that constitutively express OsARR6, a negative regulator of CK signalling
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Genes
Product Functions
References
Table 2 - Genes involved in the auxin biosynthesis, transport and signal transduction.
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OsAUX1
Auxin carrier inrice
(Xia et al., 2012)
LA1
Auxin transporter, engages in controlling the tiller angle, and
(Li et al., 2007)
suppresses auxin transportation in rice PGP
Auxin influx carrier in rice and Arabidopsis
(Xu et al., 2014 and Kramer and Bennett, 2006)
ARF
Transcription factor, inducer of auxin, expressed in coleoptiles,
(Attia et al., 2009 and
callus, and young panicles with weaker expression in leaves and
Waller et al., 2002)
roots, affects the vegetative development in rice Nal1
OsPIN1
Auxin transporter, causes stem elongation and adventitious root
(Cho et al., 2014 and Qi et
development in rice
al., 2008)
Auxin transporter and involved in controlling the tiller angle in
(Xu et al., 2005)
rice PROG1
Affects the tiller and panicle branch number and the yield of rice
(Jin et al., 2008 and Tan et
plants
al., 2008)
OsTIR1
auxin receptor genes in rice
(Xia et al., 2012)
OsYUCCA1
Exhibits an overproduction of IAA, expressed in nearly all of the
(Yamamoto et al., 2007)
organs and overlaps with the expression of a β-glucuronidase reporter gene regulated by the Auxin responsive DR5promoter in rice OsAGAP
Auxin transporter in rice
(Zhuang et al., 2006)
OsCOW1/
Auxin biosynthesis in rice
(Fujino et al., 2008 and
OsNAL7 OsNIT
Yamamoto et al., 2007) Auxin biosynthesis in rice
(Park et al., 2003)
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OsPID
Transporting auxin in rice
(Morita and Kyozuka, 2007)
OsARF1
Auxin response factor/Auxin signal transduction in rice
(Attia et al., 2009)
FISH
Auxin biosynthesis, transport and sensitivity; affects the
(Yoshikawa et al., 2014)
BONE (FIB)
pleiotropic auxin-related processes in rice
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