http://informahealthcare.com/bty ISSN: 0738-8551 (print), 1549-7801 (electronic) Crit Rev Biotechnol, Early Online: 1–10 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2014.946883

REVIEW ARTICLE

Toward understanding of rice innate immunity against Magnaporthe oryzae P. Azizi1, M. Y. Rafii1, S. N. A. Abdullah2, N. Nejat2, M. Maziah3, M. M. Hanafi2, M. A. Latif1, and M. Sahebi2

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1

Laboratory of Food Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, Serdang, Selangor, Malaysia, 2Laboratory of Plantation Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, Serdang, Selangor, Malaysia, and 3Department of Biochemistry, Faculty of Biotechnology and Biomolecular Science, Universiti Putra Malaysia, Serdang, Selangor, Malaysia Abstract

Keywords

The blast fungus, Magnaporthe oryzae, causes serious disease on a wide variety of grasses including rice, wheat and barley. The recognition of pathogens is an amazing ability of plants including strategies for displacing virulence effectors through the adaption of both conserved and variable pathogen elicitors. The pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) were reported as two main innate immune responses in plants, where PTI gives basal resistance and ETI confers durable resistance. The PTI consists of extracellular surface receptors that are able to recognize PAMPs. PAMPs detect microbial features such as fungal chitin that complete a vital function during the organism’s life. In contrast, ETI is mediated by intracellular receptor molecules containing nucleotide-binding (NB) and leucine rich repeat (LRR) domains that specifically recognize effector proteins produced by the pathogen. To enhance crop resistance, understanding the host resistance mechanisms against pathogen infection strategies and having a deeper knowledge of innate immunity system are essential. This review summarizes the recent advances on the molecular mechanism of innate immunity systems of rice against M. oryzae. The discussion will be centered on the latest success reported in plant–pathogen interactions and integrated defense responses in rice.

Basal resistance, effector-triggered immunity, pathogen, pathogen-associated molecular pattern-triggered immunity, resistance mechanisms

Introduction Food security has become an extremely important global issue, and elevations in the prices of key crops, such as rice and wheat, have occurred in recent years. The price peaks are partly due to the brunt of environmental stresses, both biotic and abiotic, that cause large losses in rice yield. Plant disease, recognized as one of the main biotic sources of these yield losses, is a constant threat to global food security. A majority of the rice diseases are caused by fungi (blast and sheath blight), bacteria (bacterial blight), nematodes (Root-knot) and viruses (rice yellow mottle virus (RYMV) (Gnanamanickam, 2009). The phytopathogenic fungus Magnaporthe oryzae is a rice blast fungus and an established plant pathogen that causes serious disease and consequently, poses a threat to the world’s most important food security crop (Talbot, 2003). M. oryzae has a vast range of host plants and is reported to infect approximately 40 species of Gramineae, comprising wheat, barley, maize, rye and millet. The main walls of plant cells are essentially a ‘‘battleground’’ between pathogens and their plant host. M. oryzae contains 30 enzymes for cellulose degradation and 44 enzymes for hemicellulose degradation of

Address for correspondence: M. Y. Rafii, Laboratory of Food Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia. E-mail: [email protected]

History Received 18 February 2014 Revised 30 May 2014 Accepted 16 June 2014 Published online 28 August 2014

plant cell walls (King et al., 2011; Wu et al., 2006). For plants to survive per se against the pathogens, complicated innate immune systems have developed where multiple defense mechanisms are activated upon infection (Dodds & Rathjen, 2010). Pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) have been reported as the two main innate immune responses in plants (Boller & He, 2009; Jones & Dangl, 2006). PTI consists of extracellular surface receptors that are able to recognize PAMPs. PAMPs protect microbial features, such as fungal chitin, that complete a vital function during the organism’s life. Thus far, a few PAMP receptors have been characterized and contain extracellular leucine-rich repeats and intracellular kinase domains (Kaku et al., 2006; Zipfel, 2008). The activation of PTI induces mitogen-activated protein (MAP) kinase signaling, transcriptional recoding mediated by WRKY-transcription factors (WRKY-TFs) and creation of reactive oxygen species (ROS) (Nurnberger & Kemmerling, 2009). These defense reactions prevent pathogen development completely. Antagonizing members of the plant specific WRKY-TFs mediate transcriptional reprogramming, which is influenced by PTI. WRKY-TF domains bind to the promoter W-box of defense genes to regulate their transcription. WRKY-TFs, as regulators, are involved in providing resistance to biotic stimuli (Yun et al., 2010). ETI, the second division of the plant immune system, consists

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of proteins encoded by resistance (R) genes that specifically identify the corresponding effector proteins produced by pathogen AVR genes (Hammond-Kosack & Kanyuka, 2007). This review summarizes the recent advances on innate immunity systems of rice plants against M. oryzae. It also delves into the latest successes reported in plant–pathogen interactions and integrated defense responses in rice.

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The PAMP/MAMP-triggered immunity system The first step of innate immunity activation relies on the specific and sensitive recognition of pathogen/microbeassociated molecular patterns (PAMPs/MAMP), such as fungal chitin and flagellin, by surface receptors, especially pattern recognition receptors (PRRs; Table 1) (Jones & Dangl, 2006; Monaghan & Zipfel, 2012; Zipfel, 2009). The PRR group includes receptor-like kinases (RLKs) and receptor-like protein (RLP). RLKs are present in the plasma membrane and contain a putative extracellular ligand-binding domain and an intracellular serine/threonine kinase domain (Shiu & Bleecker, 2001). Correspondingly, RLP includes an extracellular domain and a membrane-spanning domain. An interaction with adaptors for signal transduction is required when an intracellular activation domain is lacking (Zipfel, 2008). Some PRRs identify host damage-associated molecular patterns (DAMP), such as peptides or cell wall fragments that are released over the infection. PAMP/DAMP binding triggers PRRs and activates mechanisms of profound physiological changes in plant cells, resulting in PTI. These changes consist of calcium bursting, reactive oxygen species (ROS), mitogen-associated protein kinases (MAPKs) and calciumdependent kinase (CDPK) activation, resulting in massive transcriptional reprogramming (Nicaise et al., 2009; Tena et al., 2011). In addition to PAMPs and DAMPs, PRRs recognize conserved molecules, such as peptidoglycans (PGN), from entire microbe entities, which are known as

microbe-associated patterns (MAMPs) (Boller & Felix, 2009). An increasing susceptibility to plant disease has been reported and linked to a lack of individual PRRs (Boller & Felix, 2009). The key feature of plant innate immunity is PTI activation. The perception of MAMPs and PAMPs by PRRs leads to the creation of multiple downstream defense signaling events. To show the virulence potential of a pathogen, deactivation of PTIs using effectors is required (Bray Speth et al., 2006). Chitin and its branches, including Nacetylchito-oligosaccharides or chitin-oligosaccharides, are representative of fungal MAMP triggers in different defense responses within monocots and dicots (Antolin-Llovera et al., 2012; Shibuya & Minami, 2001). Chitin elicitor-binding protein (CEBiP), a plasma membrane glycoprotein, and OsCERK1, a Lys-M receptor kinase, are two critical components of chitin signaling in rice (Shimizu et al., 2010).

CEBiP and OsCERK1, LysM receptor fragments for CE signaling in rice Chitin normally binds to the fungal cell wall, and its fragments play the role of elicitor in various plant species. Plasma membrane chitin elicitor-binding protein (CEBiP) has been recognized as a receptor for chitin elicitor (CE) in rice. CEBiP includes two extracellular LysM domains that are attached exclusively to CE on the cell surface. Lowering the expression level of the gene encoding CEBiP leads to a decreased response to CE in rice cells. This has strongly demonstrated the importance of CEBiP in the perception and signal transduction of CE (Kaku et al., 2006). The association of CE with CEBiP leads to rice plant resistance to the blast fungus, M. oryzae; hence, improving the response to CE by engineering CEBiP enhances disease tolerance. On the other hand, the predicted structure of CEBiP does not include any functional intracellular domains for signaling through the plasma membrane into the cytoplasm (Kishimoto et al.,

Table 1. PRRs involved in rice innate immunity. Genes

Protein

Function

OsFLS2

RLK

Flagellin receptor.

OsBAK1 or BRI1-associated kinase

LRR-RK

Xa21

LRR-RLKs

CEBiP

RLP

OsCERK1 OsLYP4

RLK RLK

OsLYP6

RLK

OsRLCK185

RLCK

Pi-d2

RLK

Co-receptor of the plant hormone Brassinosteroid, which controls the resistance of rice plants against blast fungal and effects on the important agricultural traits of rice such as plant height, leaf erectness and grain morphologic features. Recognition and sensing molecule of the rice pathogen Xanthomonas oryzae. Binds chitin and interacts with the lysM-RLK CERK1 to signal intracellularly. A lysM receptor (co-receptor of CEBiP). Senses both fungal chitin and bacterial peptidoglycan (PGN) lysin motif (LysM)-containing proteins. OsLYP4 and OsLYP6, as dual functional PRRs sense bacterial peptidoglycan (PGN) and fungal chitin. Senses both fungal chitin and bacterial peptidoglycan (PGN) lysin motif (LysM)-containing proteins. OsLYP4 and OsLYP6, as dual functional PRRs sense bacterial peptidoglycan (PGN) and fungal chitin. The rice receptor-like cytoplasmic kinase, an effector of the rice pathogen Xanthomonas oryzae, acts as an essential immediate downstream signalling partner of OsCERK1 in mediating chitin- and peptidoglycan-induced plant immunity. A downstream component of OsCERK1 that itself may be a dual function receptor involved in sensing both PGN and chitin. Chimeric receptor consisting of CEBiP and Pi-d2 functions as a receptor for chitin oligosaccharides.

References (Chinchilla et al., 2007; Takai et al., 2008) (Li et al., 2009)

(Lee et al., 2009b) (Mueller & Felix, 2012) (Mueller & Felix, 2012) (Liu et al., 2012, 2013) (Liu et al., 2012, 2013) (Yamaguchi et al., 2013)

(Kouzai et al., 2013)

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2010). In rice, CEBiP forms a dimer with the chitin elicitor receptor kinase 1 (OsCERK1), also known as Lys-M-RLK1. OsCERK1 is a plasma membrane protein that contains three Lys-M motifs in its extracellular domain and an intracellular Ser/Thr-kinase domain. The OsCERK1 mutant cell line preserves some ability to respond to the elicitor in rice, either through insufficient suppression of OsCERK1 expression, or through the contribution of other OsLysM-RLKs to chitin signaling (Shimizu et al., 2010). Furthermore, OsCERK1 knockdown cell lines notably lose the ability to induce reactive oxygen species (ROS), promote the expression of defense genes or produce phytoalexins in response to CE in rice (Kishimoto et al., 2010; Okada et al., 2007). Both OsCERK1 and CEBiP have the potential to shape homo-/hetero-oligomers via the interface of their extracellular domains, while a majority of CEBiP molecules are present as homo-oligomers, even in the absence of chitin oligosaccharides. Thus, two types of LysM-containing plasma membrane proteins, CEBiP and OsCERK1, by promoting chitin elicitor signaling and activating downstream signaling, are indispensable for defense responses in rice plants.

OsRac1, a plant specific Rho-type GTPase OsRac, a small guanosine triphosphatase (GTPase) also known as ROP, belongs to the Rho-type GTPase family and is an essential regulator of innate immunity against pathogens in rice (Kawano et al., 2010b). OsRac-GTPases are molecular switches in various signal transduction pathways that control diverse cellular functions. The Rho-GTPase family plays a critical role in the regulation of disease resistance in rice. Binding of pathogen ligands by either the PAMP receptor or R protein leads to activation of Racs, which in turn spreads the signal to downstream effectors, ultimately resulting in a defense response. The Rac family comprises seven members in rice (Christensen et al., 2003), among which OsRac1 is a key regulator of the rice defense response against pathogens encoding GTPase. Over-expression analysis of the constitutively active (CA)-OsRac1 gene showed induction of ROS production and apoptosis-like cell death in rice leaves and cultured cell suspensions. In contrast, expression of a dominant negative (DN)-OsRac1 blocked ROS production and cell death, thereby confirming the importance of the OsRac1 gene for activating ROS production and regulating cell death in transgenic rice plants. In addition, CA-OsRac1 is involved in hypersensitive responses (HR), enhanced production of a phytoalexin and altered expression of defense response genes in transgenic rice lines (Ono et al., 2001). OsRac1 is also involved in the regulation of fungal sphingolipid elicitor (SE), a typical molecular PAMP, triggering rice defense responses. This implies that OsRac1 is an important regulator of rice basal immunity and plays a major role in disease resistance (Zhu et al., 2011). In recent years, the components involved in the OsRac1 signaling pathway have been characterized. These findings reveal that OsRac1 regulates ROS production via control of the NADPH oxidase (Nanda et al., 2010; Torres, 2010). Furthermore, this small GTPase adjusts the NADPH oxidase catalytic subunit of the respiratory burst oxidase homolog (Rboh) in rice to produce

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ROS (Marino et al., 2012; Suharsono et al., 2002). CAOsRac1 interacts with the N-terminus of OsRbohB through two Ca2+-binding EF-hand domains, leading to a build-up of the Ca2+ concentration that regulates this interaction. The direct interaction of Rac–Rboh might activate NADPH oxidase activity (Wong et al., 2007). On the other hand, OsRac1 most likely induces ROS generation through suppression of ROS scavengers. OsRac1 and rice blast-derived elicitors synergistically inhibit the expression of OsMT2b, a ROS scavenger gene in rice (Wong et al., 2004). These findings suggest that OsRac1 is a dual player as an inducer of ROS generation and a suppressor of ROS scavenging. OsRac1 is also markedly required for the innate immunity to blast fungus that is mediated by the Pit protein (NBS-LRR) via directly interacting with OsRac1, which is activated through pathogen infection by Pit (Kawano et al., 2010a). OsRacGEF1 has been identified as an activator and guanine nucleotide exchange factor for OsRac1. Recently, participation of an OsCEBiP/OsCERK1-OsRac1 complex in initial signaling for chitin-induced MAMP-triggered immunity (MTI) has been discovered. Further experiments revealed that OsRacGEF1 also interacts with the flagellin receptor OsFLS2 in response to rice blast (Akamatsu et al., 2013). The critical role played by GTPases such as OsRac1 has been confirmed in disease resistance findings. Nevertheless, further studies are still needed to offer a model for OsRac1-mediated signal transduction pathways in rice defense responses. A complex of molecular chaperones regulates downstream signaling in rice RAR1 and SGT1 confer disease resistance to bacterial blight and fungal blast (Wang et al., 2008). Both RAR1 and SGT1, along with Hsp90, act as chaperones via the formation of a Hsp90-RAR1-SGT1 complex that is crucial for fungal blast resistance and innate immune responses in rice (Wang et al., 2008). Furthermore, control of the OsRac1mediated immune response through the formation of a complex by two molecular chaperones, RAR1 and SGT1, has been reported. OsRAR1-RNAi rice lines indicated a decreased basal resistance to a compatible race of the fungus M. oryzae and the bacterial blight pathogen. A comparison of untransformed plants and transgenic rice plants carrying both the CA-OsRac1 and OsRAR1-RNAi constructs indicated that RAR1 is a required factor for OsRac1-mediated disease resistance in rice. OsRAR1 was similarly observed to complex with RAR1, Hsp90 and Hsp70, and it has been suggested that Hsp90 most likely helps to form a complex of OsRac1 and OsRAR1 (Thao et al., 2007). Hsp90, co-chaperone Hop/Stil, is required for chitin-triggered immune responses, while Hop/Stil interacts with OsRac1 (Chen et al., 2010). In addition, RACK1, as a scaffold protein, creates an interactive complex containing OsRac1, OsRAR1 and SCT1. This complex maintains an efficient compound that is able to turn on downstream effectors, resulting in the immune response (Figure 1).

Hetero-trimeric G proteins are a regulator of upstream signaling in rice Hetero-trimeric G proteins, a main group of signaling molecules for different cellular responses, contain three subunits, alpha (a), beta (b) and gamma (g), which are

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Figure 1. A defence complex involved in rice innate immunity.

involved in rice defense activities. Upon rice blast infection, Ga mRNA can be induced in treated rice plants. Mutation of the dwarf1 gene in rice suppressed the G gene, reduced HR, delayed R gene expression after blast infection in leaves and repressed H2O2 production upon elicitor treatment in cultured rice cells. Over-expression studies of dwarf1 in rice plants showed that CA-OsRac1 can improve H2O2 production and R gene expression. Consequently, it has been suggested that the G gene acts upstream of OsRac1 (Figure 1) (Suharsono et al., 2002). All of the results indicate the important role of the Ga gene in the rice defense system.

Transcription factors involved in immunity to blast Transcription factors such as NAC, Zn-finger, MYB, Bzip, WRKY and basic helix–loop–helix, regulators of complex traits, are involved in responses to biotic and abiotic stresses (Bhatnagar-Mathur et al., 2008; Century et al., 2008; Hu et al., 2006; Ramamoorthy et al., 2008). The large family of NAC (NAM/ATAF/CUC) genes is associated with diverse processes, including various developmental programs (Olsen et al., 2005), the formation of secondary walls (Zhong et al., 2010), senescence (Kjaersgaard et al., 2011; Yang et al., 2011), abiotic (Nakashima et al., 2012) and biotic stress responses (Christianson et al., 2010). In spite of this, only a few of them have been considered for their biological functions in disease resistance. Among 151 NAC genes in rice, only OsNAC6 (Nakashima et al., 2007), OsNAC122, OsNAC131 (Sun et al., 2013) and OsNAC19 (Lin et al., 2007b) have been characterized as increasing rice tolerance against blast disease (Nuruzzaman et al., 2010). More than 100 WRKY genes have been identified in the rice genome, out of which most are involved in innate immune responses. For instance, expression analysis confirmed that OsWRKY13 (Qiu et al., 2008), OsWRKY53 (Chujo et al., 2007), OsWRKY31 (Zhang et al., 2008), OsWRKY45 (Qiu & Yu, 2009), OsWRKY89 (Wang et al., 2007), OsWRKY82 (Peng et al., 2011), OsWRKY1 (Kim et al., 2000) and OsWRKY22 (Abbruscato et al., 2012) have important roles in resistance to blast fungal M. oryzae in rice. However, the exact roles of these genes as TFs have not yet been identified. An explanation of how WRKYs contribute by this function will

certainly soon be assisted by monitoring the interaction of specific WRKYs with DNA on a global basis. There are large groups of basic helix–loop–helix (bHLH) proteins in plants and animals; however, only a few studies have been performed with the participation of bHLH proteins in disease defense responses in plants (Lampard et al., 2008, 2009; Li et al., 2006). The PAL1 and OsWRKY19 genes are up-regulated through sphingolipid and chitin elicitors after rice blast inoculation. These two genes are regulated by bHLH-Rac Immunity1 (RAI1). According to recent findings, OsRac1, OsMKK4, OsMAPK6 and PAL1/OsWRKY19 are first temporarily expressed and activated. These components are a part of new signaling cascade that might be involved in a similar pathway in PTI against blast disease in rice (Kim et al., 2012). OsRac1 localizes to the plasma membrane (Kawano et al., 2010b), whereas OsMAPK6 and OsMAPK3 localize to the plasma membrane, cytoplasm and nucleus. It has been speculated that some of the defense components may move from the plasma membrane to the nucleus (Nakashima et al., 2008). Recently, an interaction between OsMAPK3/OsMAPK6 and OsRac1 and their important roles in the OsRac1 complex have been identified. Consequently, RAI1 is activated by OsRac1 by direct binding with OsMAPK3 and OsMAPK6 (Kim et al., 2012). Although the immune complex of OsRac1 and its function have been exactly identified, the genes involved in downstream signaling of OsRac1 have not yet been characterized. Therefore, the unveiling of such important components could help researchers to understand well this notable rice immune system.

Effector-triggered immunity system A second branch of the innate immune system in plants, known as effector-triggered immunity (ETI), was discovered to be mediated by intracellular receptor molecules containing nucleotide-binding (NB) and leucine rich repeat (LRR) domains that specifically recognize effector proteins produced by the pathogen. The binding of receptors and effectors results in the activation of defense programs and often leads to localized cell death (Chen & Ronald, 2011). In fact, ETI reactivation of defense responses is assumed to be mediated

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by the activity of cytoplasmic proteins and transcriptional reprogramming needed to make the first immune responses involving signaling from the cytoplasm to the nucleus (BurchSmith et al., 2007; Tameling & Baulcombe, 2007; Wirthmueller et al., 2007). Although PTI and ETI act as first layers of defense in plants, they are involved in disease resistance. Activation of R genes creates a faster and stronger response. The R genemediated defense response associates with the hypersensitive response (HR), a type of planned cell death. The HR occurs at the infection site and results in the restriction of both growth and the spread of pathogens to other parts of the plant. The HR is frequently accompanied by the cellular production of ROS. ROS include superoxide anions, nitrous oxide, hydrogen peroxidize, and hydroxyl radicals. ROS act as signaling molecules in plant responses, which in turn triggers a longlasting systematic response (systemic acquired resistance – SAR) that confers resistance to a broad range of pathogens (Kombrink & Schmelzer, 2001). The proteins encoded by R genes are able to recognize their cognate pathogen effectors either directly or indirectly. In plant cells, it is assumed that pathogen effectors must be localized inside the cell, as the majority of R proteins are intracellular. In spite of pathogen diversity, a large number of R genes can be grouped into one large family. This gene family encodes Nucleotide Binding Site (NBS) proteins with C-terminal Leucine Rich Repeat (LRR) domains, except Pid2 and Pi21, which encode a receptor-like kinase (Chen et al., 2006) and proline-rich protein (Fukuoka et al., 2009), respectively. The NBS-LRR proteins are subdivided into two subgroups based on distinct N-terminal domains. One group contains a coiled coil (CC) domain, while the other has homology to the cytosolic portion of TOLL/interleukin-1 receptors (Dangl & Jones, 2001). In recent years, a wide range of progress has been made in investigating the molecular mechanisms of innate immunity responses in rice, as well as the identification of R genes (Table 2), identification-triggered early signaling, signaling pathways in rice and the role of these signaling pathways in activating defense responses (Liu et al., 2010; Saitoh et al., 2012; Seo et al. 2011; Valent & Khang, 2010). However, a complete understanding of the molecular network regulating defense responses against pathogens in rice is still obscured. For instance, despite the number of R genes present in rice, little is known about the essential signaling needed to initiate effector-triggered resistance against pathogens (e.g. M. oryzae). Rice blast immunity is categorized in a gene-forgene system. The theory of this system was raised by Harold H Flor in the 1940s. It explains how Avr genes within the pathogen connect to particular R genes in rice and how the absence of R genes will make rice susceptible (Zeigler et al., 1994). Certain molecules, known as effectors, are produced by phytopathogens and encoded by virulence genes (Avr). These effectors are delivered directly into plant cells during the primary stage of infection and change host plant physiology. Effectors are used to promote pathogen colonization or interrupt the activation of host cells defenses. On the other hand, rice plants have consequently responded with a form of immunity that is based on the sensitivity of effectors to host resistance proteins. This immunity is called the genefor-gene system (Hammond-Kosack & Kanyuka, 2007).

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Table 2. List of cloned genes involved in rice immunity against blast disease. Genes Pib

Location

OsWRKY13 OsWRKY45

The long arm of chromosome 2 On chromosome 12 The long arm of chromosome 11 Near the centromere chromosome 6 Near the centromere chromosome 6 Near the centromere chromosome 6 Near the centromere chromosome 6 On chromosome 8 On chromosome 1 On the long arm of chromosome 11 On chromosome 9 On chromosome 4 On chromosome 1 On chromosome 6 On chromosome 1 On chromosome 11 On chromosome 11 On chromosome 11 On chromosome 6 On chromosome 11 The long arm of chromosome 2 On chromosome 1 On chromosome 5

OsWRKY22 OsWRKY76 OsWRKY89 OsNAC122 OsNAC131 OsNAC6 OsNAC19

On chromosome 1 On chromosome 2 On chromosome 12 – – – –

Pita Pi-kh (Pi54) Pid2 Pi9 Pizt Pi2 Pi36 Pi37 Pi-km Pi5 Pi21 Pit Pid3 Pish Pik Pik-p Pia Pi25 Pi1 Pib

References (Wang et al., 1999) (Bryan et al., 2000) (Sharma et al., 2005) of

(Chen et al., 2006)

of

(Qu et al., 2006)

of

(Zhou et al., 2006)

of

(Zhou et al., 2006) (Liu et al., 2007) (Lin et al., 2007a) (Ashikawa et al., 2008) (Lee et al., 2009a) (Fukuoka et al., 2009) (Hayashi & Yoshida, 2009) (Shang et al., 2009) (Takahashi et al., 2010) (Zhai et al., 2011) (Yuan et al., 2011) (Okuyama et al., 2011) (Chen et al., 2011) (Hua et al., 2012) (Wang et al., 1999) (Wen et al., 2003) (Shimono et al., 2007; Tao et al., 2009) (Abbruscato et al., 2012) (Yokotani et al., 2013) (Wang et al., 2007) (Sun et al., 2013) (Sun et al., 2013) (Nakashima et al., 2007) (Lin et al., 2007b)

Before pathogen action, ‘‘trigger’’ and ‘‘target’’ proteins are placed at the plasma membrane. An NBS-LRR protein and adaptor, accompanied by downstream signaling proteins, creates the trigger complex, responsible for its negative regulation. The target protein complex includes the same adaptor and putative signaling components. After infection, the pathogen effectors bind to the target complex and modify the adaptor. Displacement of the negative regulator and other downstream signaling are the result of the relationship between modified target and trigger complexes. At this time, the trigger complex undergoes conformational modifications, making it ready for action (Figure 2) (Belkhadir et al., 2004; Bonardi & Dangl, 2012).

Avr and non-Avr effectors Magnaporthe oryzae produces effector proteins to influence plant immunity and physiology systems, leading to the penetration of infection. Avr proteins are a special group of effectors encoded by avirulence genes (Table 3). These proteins can be distinguished by relative R proteins and leads to the race-specific recognition (de Wit et al., 2009; Djamei & Kahmann, 2012). Over 40 Avr genes have been identified, with all of them except ACE1 encoding secreted proteins in

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Figure 2. A schematic figure of rice innate immunity against M. oryzae. PTI: identification of different effectors by PRRs in response to infection. Rectangles and triple circles (Pid2, CEBiP, FLS2, OsBAK1, CERK1, LRR (Xa21) and OsLYP4/6) are involved in PRRs group. K: Kinase domain; Flag: Flagellin. ETI: inner immunity of rice after blast infection by activation of the NBS-LRR protein complex. Block arc: Block arc as downstream signalling proteins.

invasive hyphae. ACE1 encodes an intracellular hybrid protein known as PKS-NRPS (Bohnert et al., 2004). The expression of Avr-Piz-t suppresses PAMP-triggered immunity by hindering the ubiquitin ligase activity of the rice RING E3 ubiquitin ligase APIP6 (Park et al., 2012). In addition, a putative neutral zinc metalloprotease is encoded by Avr-Pita gene (Jia et al., 2000). PWL1 and PWL2 belong to another Avr gene family that functions in the avirulence protein infection of weeping love grass. Avr1-CO39 is specifically expressed in invasive hyphae and triggers HR and resistance in cultivars containing the Pi-CO39 gene (Peyyala & Farman, 2006). AvrPia, Avr-Pik/km/kp and Avr-Pii were characterized in the same study of the M. oryzae strain Ina168 (Yoshida et al., 2009). Recently, interactions between Avr-Pia and Avr1CO39, as well as direct interactions of Avr-Pia with Rga5-A, have been discovered (Cesari et al., 2013). Slp1, the best example of a non-Avr effector in Magnaporthe oryzae, is required for invasive growth of appressorium in plants. It gathers at the interface between invasive hyphae and extra-

invasive-hyphal membranes and competes with CEBiP for binding to chitin oligosaccharides (Mentlak et al., 2012). BAS1-4 and MC69 encode secreted proteins specifically expressed in invasive hyphae (Mosquera et al., 2009; Saitoh et al., 2012). The encoding of the 54-aa MC69 protein is vital for invasive hyphae, although it is not transferred into the rice cytoplasm (Zhang & Xu, 2014).

Conclusions Plants have developed innate immune systems to combat biotic stresses. Meanwhile, pathogens have evolved effector proteins that suppress host immune responses. Numerous fascinating findings have been achieved on the rice-M. Oryzae interactions, for instance, the identification of Avr effectors by R genes that quickly activate a coalesced immune response in rice cells. Several important outcomes have been discovered, such as ROS generation, PR gene activation and hormone biosynthesis. However, the associations and components

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Table 3. Characteristics of Avr and non-Avr effectors in M. oryzae. Avr and Non-Avr effectors

Protein coding sequence

Function

References

Glycine-rich, hydrophilic protein, Secreted protein Glycine-rich, hydrophilic protein, Secreted protein Secreted protein Secreted protein

Confers avirulence of the Eleusine isolate, Function as avirulence proteins of weeping love grass. Confers avirulence of the Oryza isolate, Function as avirulence proteins of weeping love grass. Diagnosed by Pi-ta (R protein). Diagnosed by PiCo39 (R protein). Diagnosed by Pi33 (R protein).

Avr Pizt Avr-Pia

Polyketide synthase (Peptide synthetase) Secreted protein Secreted protein

(Kang et al., 1995; Sweigard et al., 1995) (Kang et al., 1995; Sweigard et al., 1995) (Orbach et al., 2000) (Leong, 2008; Ribot et al., 2013) (Bohnert et al., 2004)

Avr Pii Avr Pik/km/kp BAS1

Secreted protein Secreted protein Secreted protein

BAS2

Secreted protein

BAS3 BAS4 SLP1

Secreted protein Secreted protein Secreted protein

MC69

Secreted protein

MoCDIP1-5

Secreted protein

PWL1 PWL2 Avr Pi-ta Avr1-Co39

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ACE1

Diagnosed by Pizt (R protein). Diagnosed by Pia (R protein). Diagnosed by Pii (R protein). Diagnosed by Pik/km/kp (R protein). Accumulated in biotrophic interfacial complexes along with known avirulence effector. Accumulated in biotrophic interfacial complexes along with known avirulence effector. Localised near cell wall crossing point. Outlined growing invasive hyphae. Functions to suppress chitin-induced plant immune responses, involving generation of reactive oxygen species and expression of defence related genes. Necessary for fungus infection and development of invasive hyphae after appressorium formation in rice leaf sheath. Induce plant cell death in a transient expression assay with rice protoplasts.

involved in immune responses utilizing R genes are still unknown in rice. Similarly, there is a lack of clarity concerning the ability of OsCERK1 to directly bind chitin oligosaccharides with the high affinity needed for the functional receptor of the chitin oligosaccharide elicitor. However, the important role of CEBiP in chitin elicitor binding and OsCERK1 functions as a signal transducer through its Ser/Thr activity is clear in rice. This study provides an understanding of the fundamental principles of rice-M. oryzae interactions. However, many details need to be clarified concerning the innate immunity system against diseases in rice, such as how WRKY-TFs function in diverse metabolic pathways or how pathogens impinge on the vast network of plants to counter host defenses and make use of it for their individual preferences. Clearly, an improved understanding of plant–pathogen interactions and the molecular details of plant defense mechanisms will enable us to improve and manage the plant immune system against potential enemies such as diseases.

Declaration of interest The authors report no declarations of interest. The authors wish to acknowledge the Long-Term Research Grant Scheme (LRGS), Food Security project (Grant No. 5525001), Ministry of Education, Malaysia, for financial support.

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