Editorial
Receptor-like Kinases: Key Regulators of Plant Development and Defense
Jia Li1a, Frans E. Tax2a
1
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences,
Lanzhou University, Lanzhou 730000, China 2
Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721-0036, USA
a
Special Issue Editor
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: [10.1111/jipb.12129] This article is protected by copyright. All rights reserved.
1
Plants are multi-cellular organisms that live in diverse and fluctuating environments. Cell-cell and cell-environment communication are therefore critical to plant growth and development. In animals, transmembrane receptor protein tyrosine kinases play significant roles in cell-cell signaling. There was a great deal of surprise in the plant community, however, when the first receptor-like protein kinase (RLK) was isolated from maize by John Walker and Ren Zhang (1990) over twenty years ago, because plant cells contain cell walls which were thought to be more rigid and less dynamic than the extracellular matrix of animal cells. Researchers were also initially skeptical that small signaling molecules (ligands) could freely move through cell walls to deliver signals. The identification of RLKs from plants suggested that plants utilize mechanisms similar to animals in cell-cell communication. Genome sequencing revealed that plant genomes encode a great number of RLKs, much more than in animals. For example, the Arabidopsis genome possesses around 610 RLK coding sequences (Shiu and Bleecker 2001a, 2001b), whereas the rice genome contains almost twice the number found in Arabidopsis (Shiu et al. 2004). A typical RLK contains an extracellular domain, a single-pass transmembrane domain, and a cytoplasmic kinase domain. Usually the extracellular domain of a ligand-binding RLK physically interacts with a small ligand molecule, one either secreted from surrounding cells or presented as a conserved pathogen associated molecular pattern (PAMP), which triggers or secures the homo- or hetero-dimerization of two RLK molecules, leading to mutual phosphorylation of both RLKs. The activated RLKs then transduce the signal to downstream networks and eventually alter gene transcription patterns, establishing a cellular response to the specific ligand. Based on their characterized biological roles thus far, most RLKs can be categorized functionally into two groups, those that have roles in development or those that function in defense. Some RLKs, however, play dual roles in both development and defense. In this special issue, up-to-date mechanistic details of several RLKs in regulating plant development and defense are discussed (He et al. 2013; Jiang et al. 2013; Lin et al. 2013; Niederhuth et al. 2013; Shpak 2013; Wierzba and Tax 2013; Wu and Zhou 2013; Zhang and Thomma 2013). 2
RLKs and Plant Development
Although hundreds of RLKs have been identified in many plant species, so far only around fifty of them have been functionally characterized. Most of the characterized RLKs belong to the largest subfamily of RLKs, named leucine-rich repeat receptor-like protein kinases (LRR-RLKs) based on their extracellular domains (Shiu and Bleecker 2001a, 2001b, 2003). RLKs mediate a wide range of physiological processes during normal growth and development, from zygotic embryogenesis to flowering. For instance, BAM1/2, EMS1, FER, SERK1/2, and RPK2/TOAD2 are involved in anther development and fertilization (Zhao et al. 2002; Albrecht et al. 2005; Colcombet et al. 2005; Hord et al. 2006; Escobar-Restrepo et al. 2007; Mizuno et al. 2007); PXY/TDR controls xylem differentiation (Fisher and Turner 2007; Hirakawa et al. 2010); BAM1/2, CLV1, RPK2, and CRN regulate shoot apical meristem maintenance and development (Clark et al. 1997; DeYoung et al. 2006; Müller et al. 2008; Kinoshita et al. 2010); ERECTA, ERL1, ERL2, and PSKR mediate plant architecture, cell proliferation and organ growth (Torii et al. 1996; Matsubayashi et al. 2002; Shpak et al. 2003); BRI1, BRL1, BRL3, BAK1, SERK1, and BKK1 are the receptors and co-receptors for brassinosteroids (BRs), regulating BR perception and signal initiation (Li et al. 2002; Nam and Li 2002; Karlova et al. 2006; He et al. 2007; Gou et al. 2012; Santiago et al. 2013; Sun et al. 2013); ERECTA, ERL1, and ERL2 also control stomatal development (Shpak et al. 2005; Lee et al. 2012). SERK1, SERK2, BAK1, and BKK1 not only regulate BR signaling but also regulate BR-independent cell-death and root developmental pathways (He et al. 2007; Li 2010; Du et al. 2012); RPK1/TOAD2, ACR4/ALE2, GSO1/GSO2 are involved in zygotic embryogenesis (Tanaka et al. 2002; Nodine et al. 2007; Tsuwamoto et al. 2008). There are also still many secreted proteins that could be ligands for RLKs. For example, polypeptides called LUREs were found to be secreted from synergid cells for pollen tube guidance (Okuda et al. 2009), and it was proposed that their cognate RLKs are located on the tips of pollen tubes to control fertilization. However the responsible RLKs still need to be identified. 3
RLKs and Plant Defense
Several receptor-like kinases have been found to be involved in pathogen recognition. Typically, plants detect invading pathogens by recognizing conserved signatures called Pathogen Associated Molecular Patterns, or PAMPs. RLKs directly perceiving PAMPs are called pattern recognition receptors (PRRs). FLS2 and EFR are the two best characterized PRRs, binding to the PAMPs flag 22 and EF-Tu, respectively (Gómez-Gómez and Boller 2000; Zipfel et al. 2006). When the extracellular domain of a PRR binds a PAMP, a downstream innate immune response is triggered. In addition to PRRs, recent studies have also revealed that some RLKs such as BAK1 and BKK1 can act as co-receptors of FLS2 and EFR to mediate their corresponding signaling pathways (Chinchilla et al. 2007; Heese et al. 2007; Boller and Felix 2009). Other recent studies have also uncovered that some RLKs are involved in abiotic stress responses. For example, the expression of RPK1 is induced by drought, ABA, high salt and low temperature. Loss-of-function genetic analyses indicated that RPK1 is involved in ABA-related stress responses (Osakabe et al. 2005). GHR1 is another RLK which responds to ABA and H2O2 mediated stomatal movement (Hua et al. 2012). There are still numerous RLKs whose expression is induced by either biotic or abiotic stress, but their specific roles in regulating defense responses need to be characterized in the future.
Future Perspectives
Genetic analyses have revealed the roles of a small fraction of RLKs. Most are yet to be functionally defined. For those whose functions are already known, the detailed molecular mechanisms are still not completely 4
understood. One of the greatest challenges regarding RLK-mediated signaling pathways is the identification of ligands. In addition, due to functional redundancy, it is difficult to uncover the functions of many RLKs. Furthermore, some RLKs are involved in multiple signaling pathways. For example, BAK1 regulates the BR signaling pathway to promote growth (Li et al. 2002; Nam and Li 2002). BAK1 also acts as a co-receptor in FLS2- and EFR-mediated signaling pathways to induce defense responses (Chinchilla et al. 2007; Heese et al. 2007). This makes biological sense as switching on defense responses causes the reduction of growth. In fact, BAK1 may be involved in multiple pathways distinct from the ones already uncovered. An outstanding question is how BAK1 and its other co-receptors are able to regulate multiple signaling pathways, especially those leading to opposite biological consequences. Genetics, biochemical “omics”, and other novel technologies will be useful to ultimately elucidate these questions in the near future. The knowledge obtained from these studies will contribute significantly to our better understanding of the big picture of plant growth and development, and to future genetic engineering-based crop improvements for higher productivity, including better adaptations to various biotic and abiotic stresses.
5
References
Albrecht C, Russinova E, Hecht V, Baaijens E, Vries SD (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17, 3337-3349. Boller T, Felix G (2009) A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Physiol. 60, 379-406. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497-500. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350-3361. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptorkinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16. Du J, Yin H, Zhang S, Wei Z, Zhao B, Zhang J, Gou X, Lin H, Li J (2012) Somatic embryogenesis receptor kinases control root development mainly via brassinosteroid-independent actions in Arabidopsis thaliana. J. Integr. Plant Biol. 54, 388-399. Escobar-Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317, 456-460. Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17, 1061-1066. Gómez-Gómez L, Boller T (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011. Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, D.Clouse S, Li J (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8, e1002452. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida h, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 6
1109-1115. He K, Xu S, Li J (2013) BAK1 directly regulates brassinosteroid perception and BRI1 activation. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12122. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104, 12217–12222. Hirakawa Y, Kondo Y, Fukuda H (2010) Regulation of vascular development by CLE peptide-receptor systems. J. Integr. Plant Biol. 52, 8-16. Hord CLH, Chen C, DeYoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1167-1180. Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546-2561. Jiang J, Zhang C, Wang X (2013) Ligand perception, activation, and early signaling of plant steroid receptor brassinosteroid insensitive. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12081. Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, Vries SD (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18, 626-638. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911-3920. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, McAbee JM, Sarikaya M, Tamerler C, Torii KU (2012) Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev. 26, 126-136. Li J (2010) Multi-tasking of somatic embryogenesis receptor-like protein kinases. Curr. Opin. Plant Biol. 13, 509-514. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222. Lin W, Ma X, Shan L, He P (2013) Big roles of small kinases: The complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12071. Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296, 1470-1472. 7
Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 50, 751-766. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212. Niederhuth CE, Cho SK, Seitz K, Walker JC (2013) Letting go is never easy: Abscission and receptor-like protein kinases. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12116. Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev. Cell 12, 943-956. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357-361. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K (2005) Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17, 1105-1119. Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by smatic embryogenesis co-receptor kinases. Science 341, 889-892. Shiu S-H, Bleecker AB (2001a) Plant receptor-like kinase gene family: Diversity, function, and signaling. Sci. Signal. 2001, re22. Shiu S-H, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98, 10763–10768. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530–543. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234. Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15, 1095-1110. Shpak ED (2013) Diverse roles of ERECTA family genes in plant development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12108. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309, 290-293. 8
Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765-777. Sun Y, Han Z, Tang J, Hu Z, Chai C, Zhou B, Chai J (2013) Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res. doi: 10.1038/cr.2013.131. Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol. 43, 419-428. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735-746. Tsuwamoto R, Fukuoka H, Takahata Y (2008) GASSHO1 and GASSHO2 encoding a putative leucine-richrepeat transmembrane-type receptor kinase are essentialfor the normal development of the epidermal surface in Arabidopsis embryos. Plant J. 54, 30-42. Wierzba MP, Tax FE (2013) Notes from the underground: Receptor-like kinases in Arabidopsis root development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12088. Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12123. Zhang Z, Thomma BPHJ (2013) Structure-function aspects of extracellular leucine-rich repeat-containing cell surface receptors in plants. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12080. Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760.
9
Receptor-like Kinases: Key Regulators of Plant Development and Defense
Jia Li1a, Frans E. Tax2a
1
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences,
Lanzhou University, Lanzhou 730000, China 2
Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721-0036, USA
a
Special Issue Editor
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: [10.1111/jipb.12129] This article is protected by copyright. All rights reserved.
1
Plants are multi-cellular organisms that live in diverse and fluctuating environments. Cell-cell and cell-environment communication are therefore critical to plant growth and development. In animals, transmembrane receptor protein tyrosine kinases play significant roles in cell-cell signaling. There was a great deal of surprise in the plant community, however, when the first receptor-like protein kinase (RLK) was isolated from maize by John Walker and Ren Zhang (1990) over twenty years ago, because plant cells contain cell walls which were thought to be more rigid and less dynamic than the extracellular matrix of animal cells. Researchers were also initially skeptical that small signaling molecules (ligands) could freely move through cell walls to deliver signals. The identification of RLKs from plants suggested that plants utilize mechanisms similar to animals in cell-cell communication. Genome sequencing revealed that plant genomes encode a great number of RLKs, much more than in animals. For example, the Arabidopsis genome possesses around 610 RLK coding sequences (Shiu and Bleecker 2001a, 2001b), whereas the rice genome contains almost twice the number found in Arabidopsis (Shiu et al. 2004). A typical RLK contains an extracellular domain, a single-pass transmembrane domain, and a cytoplasmic kinase domain. Usually the extracellular domain of a ligand-binding RLK physically interacts with a small ligand molecule, one either secreted from surrounding cells or presented as a conserved pathogen associated molecular pattern (PAMP), which triggers or secures the homo- or hetero-dimerization of two RLK molecules, leading to mutual phosphorylation of both RLKs. The activated RLKs then transduce the signal to downstream networks and eventually alter gene transcription patterns, establishing a cellular response to the specific ligand. Based on their characterized biological roles thus far, most RLKs can be categorized functionally into two groups, those that have roles in development or those that function in defense. Some RLKs, however, play dual roles in both development and defense. In this special issue, up-to-date mechanistic details of several RLKs in regulating plant development and defense are discussed (He et al. 2013; Jiang et al. 2013; Lin et al. 2013; Niederhuth et al. 2013; Shpak 2013; Wierzba and Tax 2013; Wu and Zhou 2013; Zhang and Thomma 2013). 2
RLKs and Plant Development
Although hundreds of RLKs have been identified in many plant species, so far only around fifty of them have been functionally characterized. Most of the characterized RLKs belong to the largest subfamily of RLKs, named leucine-rich repeat receptor-like protein kinases (LRR-RLKs) based on their extracellular domains (Shiu and Bleecker 2001a, 2001b, 2003). RLKs mediate a wide range of physiological processes during normal growth and development, from zygotic embryogenesis to flowering. For instance, BAM1/2, EMS1, FER, SERK1/2, and RPK2/TOAD2 are involved in anther development and fertilization (Zhao et al. 2002; Albrecht et al. 2005; Colcombet et al. 2005; Hord et al. 2006; Escobar-Restrepo et al. 2007; Mizuno et al. 2007); PXY/TDR controls xylem differentiation (Fisher and Turner 2007; Hirakawa et al. 2010); BAM1/2, CLV1, RPK2, and CRN regulate shoot apical meristem maintenance and development (Clark et al. 1997; DeYoung et al. 2006; Müller et al. 2008; Kinoshita et al. 2010); ERECTA, ERL1, ERL2, and PSKR mediate plant architecture, cell proliferation and organ growth (Torii et al. 1996; Matsubayashi et al. 2002; Shpak et al. 2003); BRI1, BRL1, BRL3, BAK1, SERK1, and BKK1 are the receptors and co-receptors for brassinosteroids (BRs), regulating BR perception and signal initiation (Li et al. 2002; Nam and Li 2002; Karlova et al. 2006; He et al. 2007; Gou et al. 2012; Santiago et al. 2013; Sun et al. 2013); ERECTA, ERL1, and ERL2 also control stomatal development (Shpak et al. 2005; Lee et al. 2012). SERK1, SERK2, BAK1, and BKK1 not only regulate BR signaling but also regulate BR-independent cell-death and root developmental pathways (He et al. 2007; Li 2010; Du et al. 2012); RPK1/TOAD2, ACR4/ALE2, GSO1/GSO2 are involved in zygotic embryogenesis (Tanaka et al. 2002; Nodine et al. 2007; Tsuwamoto et al. 2008). There are also still many secreted proteins that could be ligands for RLKs. For example, polypeptides called LUREs were found to be secreted from synergid cells for pollen tube guidance (Okuda et al. 2009), and it was proposed that their cognate RLKs are located on the tips of pollen tubes to control fertilization. However the responsible RLKs still need to be identified. 3
RLKs and Plant Defense
Several receptor-like kinases have been found to be involved in pathogen recognition. Typically, plants detect invading pathogens by recognizing conserved signatures called Pathogen Associated Molecular Patterns, or PAMPs. RLKs directly perceiving PAMPs are called pattern recognition receptors (PRRs). FLS2 and EFR are the two best characterized PRRs, binding to the PAMPs flag 22 and EF-Tu, respectively (Gómez-Gómez and Boller 2000; Zipfel et al. 2006). When the extracellular domain of a PRR binds a PAMP, a downstream innate immune response is triggered. In addition to PRRs, recent studies have also revealed that some RLKs such as BAK1 and BKK1 can act as co-receptors of FLS2 and EFR to mediate their corresponding signaling pathways (Chinchilla et al. 2007; Heese et al. 2007; Boller and Felix 2009). Other recent studies have also uncovered that some RLKs are involved in abiotic stress responses. For example, the expression of RPK1 is induced by drought, ABA, high salt and low temperature. Loss-of-function genetic analyses indicated that RPK1 is involved in ABA-related stress responses (Osakabe et al. 2005). GHR1 is another RLK which responds to ABA and H2O2 mediated stomatal movement (Hua et al. 2012). There are still numerous RLKs whose expression is induced by either biotic or abiotic stress, but their specific roles in regulating defense responses need to be characterized in the future.
Future Perspectives
Genetic analyses have revealed the roles of a small fraction of RLKs. Most are yet to be functionally defined. For those whose functions are already known, the detailed molecular mechanisms are still not completely 4
understood. One of the greatest challenges regarding RLK-mediated signaling pathways is the identification of ligands. In addition, due to functional redundancy, it is difficult to uncover the functions of many RLKs. Furthermore, some RLKs are involved in multiple signaling pathways. For example, BAK1 regulates the BR signaling pathway to promote growth (Li et al. 2002; Nam and Li 2002). BAK1 also acts as a co-receptor in FLS2- and EFR-mediated signaling pathways to induce defense responses (Chinchilla et al. 2007; Heese et al. 2007). This makes biological sense as switching on defense responses causes the reduction of growth. In fact, BAK1 may be involved in multiple pathways distinct from the ones already uncovered. An outstanding question is how BAK1 and its other co-receptors are able to regulate multiple signaling pathways, especially those leading to opposite biological consequences. Genetics, biochemical “omics”, and other novel technologies will be useful to ultimately elucidate these questions in the near future. The knowledge obtained from these studies will contribute significantly to our better understanding of the big picture of plant growth and development, and to future genetic engineering-based crop improvements for higher productivity, including better adaptations to various biotic and abiotic stresses.
5
References
Albrecht C, Russinova E, Hecht V, Baaijens E, Vries SD (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17, 3337-3349. Boller T, Felix G (2009) A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Physiol. 60, 379-406. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497-500. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350-3361. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptorkinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16. Du J, Yin H, Zhang S, Wei Z, Zhao B, Zhang J, Gou X, Lin H, Li J (2012) Somatic embryogenesis receptor kinases control root development mainly via brassinosteroid-independent actions in Arabidopsis thaliana. J. Integr. Plant Biol. 54, 388-399. Escobar-Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317, 456-460. Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17, 1061-1066. Gómez-Gómez L, Boller T (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011. Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, D.Clouse S, Li J (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8, e1002452. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida h, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 6
1109-1115. He K, Xu S, Li J (2013) BAK1 directly regulates brassinosteroid perception and BRI1 activation. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12122. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104, 12217–12222. Hirakawa Y, Kondo Y, Fukuda H (2010) Regulation of vascular development by CLE peptide-receptor systems. J. Integr. Plant Biol. 52, 8-16. Hord CLH, Chen C, DeYoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1167-1180. Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546-2561. Jiang J, Zhang C, Wang X (2013) Ligand perception, activation, and early signaling of plant steroid receptor brassinosteroid insensitive. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12081. Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, Vries SD (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18, 626-638. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911-3920. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, McAbee JM, Sarikaya M, Tamerler C, Torii KU (2012) Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev. 26, 126-136. Li J (2010) Multi-tasking of somatic embryogenesis receptor-like protein kinases. Curr. Opin. Plant Biol. 13, 509-514. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222. Lin W, Ma X, Shan L, He P (2013) Big roles of small kinases: The complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12071. Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296, 1470-1472. 7
Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 50, 751-766. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212. Niederhuth CE, Cho SK, Seitz K, Walker JC (2013) Letting go is never easy: Abscission and receptor-like protein kinases. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12116. Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev. Cell 12, 943-956. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357-361. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K (2005) Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17, 1105-1119. Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by smatic embryogenesis co-receptor kinases. Science 341, 889-892. Shiu S-H, Bleecker AB (2001a) Plant receptor-like kinase gene family: Diversity, function, and signaling. Sci. Signal. 2001, re22. Shiu S-H, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98, 10763–10768. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530–543. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234. Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15, 1095-1110. Shpak ED (2013) Diverse roles of ERECTA family genes in plant development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12108. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309, 290-293. 8
Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765-777. Sun Y, Han Z, Tang J, Hu Z, Chai C, Zhou B, Chai J (2013) Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res. doi: 10.1038/cr.2013.131. Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol. 43, 419-428. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735-746. Tsuwamoto R, Fukuoka H, Takahata Y (2008) GASSHO1 and GASSHO2 encoding a putative leucine-richrepeat transmembrane-type receptor kinase are essentialfor the normal development of the epidermal surface in Arabidopsis embryos. Plant J. 54, 30-42. Wierzba MP, Tax FE (2013) Notes from the underground: Receptor-like kinases in Arabidopsis root development. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12088. Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12123. Zhang Z, Thomma BPHJ (2013) Structure-function aspects of extracellular leucine-rich repeat-containing cell surface receptors in plants. J. Integr. Plant Biol. 55, DOI: 10.1111/jipb.12080. Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760.
9
