Plant Mol Biol (2009) 69:473–488 DOI 10.1007/s11103-008-9435-0
Role of plant hormones in plant defence responses Rajendra Bari Æ Jonathan D. G. Jones
Received: 5 August 2008 / Accepted: 12 November 2008 / Published online: 16 December 2008 Ó Springer Science+Business Media B.V. 2008
Abstract Plant hormones play important roles in regulating developmental processes and signaling networks involved in plant responses to a wide range of biotic and abiotic stresses. Significant progress has been made in identifying the key components and understanding the role of salicylic acid (SA), jasmonates (JA) and ethylene (ET) in plant responses to biotic stresses. Recent studies indicate that other hormones such as abscisic acid (ABA), auxin, gibberellic acid (GA), cytokinin (CK), brassinosteroids (BR) and peptide hormones are also implicated in plant defence signaling pathways but their role in plant defence is less well studied. Here, we review recent advances made in understanding the role of these hormones in modulating plant defence responses against various diseases and pests. Keywords Hormones Plant defence Pathogen Virulence Signaling Peptide Biotrophs Necrotrophs
Introduction In their natural environment, plants encounter a vast array of pathogenic microorganisms such as fungi, oomycetes, bacteria, viruses and nematodes. These diverse pathogens deliver effector molecules (also called virulence factors) into the plant cell to promote virulence and cause disease. Despite the presence of a large number of microorganisms in the surroundings of plants, few microorganisms are able R. Bari J. D. G. Jones (&) The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK e-mail: [email protected]
R. Bari e-mail: [email protected]
to attack any particular plant species. Plants are able to protect themselves against microbes and disease is the exception rather than the rule. Plant defence mechanisms are usually complex and composed of multiple layers of defence that are effective against diverse array of pathogens. Plants utilize preformed physical and chemical barriers that hinder pathogen entry and infection. In addition, plants have evolved a wide variety of inducible defence mechanisms that are triggered upon pathogen recognition. These inducible defences include multifaceted molecular, biochemical, and morphological changes, such as oxidative burst, expression of defence-related genes, production of antimicrobial compounds, and/or programmed cell death (van Loon et al. 2006). Plants defend themselves against most potential microbial pathogens through a basal defence mechanism (also called innate immune system). The current view of the plant immune system has been represented as a ‘zigzag’ model in which the perception of microbial- or pathogenassociated molecular patterns (MAMPs or PAMPs) by host encoded pattern recognition receptors (PRRs) results in PAMP triggered immunity (PTI). Successful pathogens secrete effectors that suppress PTI and thus induce disease resulting in effector triggered susceptibility (ETS). As a counter defence strategy, plants recognise a given effector either directly or indirectly and activate effector-triggered immunity (ETI) resulting in disease resistance (Chisholm et al. 2006; Jones and Dangl 2006). The activation of PTI or ETI enhances plant disease resistance and restricts pathogen growth. Hence, the timely recognition of an invading microorganism coupled with the rapid and effective induction of defence responses appears to make a key difference between resistance and susceptibility. Plants produce a wide variety of hormones, which include auxins, gibberellins (GA), abscisic acid (ABA),
cytokinins (CK), salicylic acid (SA), ethylene (ET), jasmonates (JA), brassinosteroids (BR) and peptide hormones. Recently, strigolactones are identified as a new class of plant hormones (Gomez-Roldan et al. 2008; Umehara et al. 2008). Plant hormones play important roles in diverse growth and developmental processes as well as various biotic and abiotic stress responses in plants. Infection of plants with diverse pathogens results in changes in the level of various phytohormones (Adie et al. 2007; RobertSeilaniantz et al. 2007). The identification and characterization of several mutants affected in the biosynthesis, perception and signal transduction of these hormones has been instrumental in understanding the role of individual components of each hormone signaling pathway in plant defence. Substantial progress has been made in understanding individual aspects of phytohormone perception, signal transduction, homeostasis or influence on gene expression. However, the underlying molecular mechanisms by which plants integrate stress induced changes in hormone levels and initiate adaptive responses are poorly understood. Microbial pathogens have also developed the ability to manipulate the defence-related regulatory network of plants by producing phytohormones or their functional mimics. This results in hormonal imbalance and activation of inappropriate defence responses (Robert-Seilaniantz et al. 2007). For example, production of coronatine—a JA-Ile mimic by Pseudomonas syringae pv. tomato (Pst) bacteria, triggers the activation of JA-dependent defence responses leading to the suppression of SA-dependent defence responses and promotion of disease symptoms (Cui et al. 2005; Laurie-Berry et al. 2006). In addition, coronatine has been shown to prevent PAMP-induced stomatal closure which facilitates bacterial entry into the leaf (Melotto et al. 2006). However, we still have limited knowledge on complex regulatory networks where multiple hormonal pathways interact and influence plant defence responses. This review focuses on major recent advances made in the identification of different hormonal components involved in defence responses of plants against various pests and diseases.
Salicylic acid, jasmonates and ethylene Three phytohormones—SA, JA and ET, are known to play major roles in regulating plant defence responses against various pathogens, pests and abiotic stresses such as wounding and exposure to ozone (Glazebrook 2005; Lorenzo and Solano 2005; Broekaert et al. 2006; Loake and Grant 2007; Balbi and Devoto 2008). SA plays a crucial role in plant defence and is generally involved in the activation of defence responses against biotrophic and hemi-biotrophic pathogens as well as the establishment of
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systemic acquired resistance (SAR, Grant and Lamb 2006). Mutants that are affected in the accumulation of SA or are insensitive to SA show enhanced susceptibility to biotrophic and hemi-biotrophic pathogens. Recently, it has been shown that, methyl salicylate, which is induced upon pathogen infection, acts as a mobile inducer of SAR in tobacco (Park et al. 2007). SA levels increase in pathogenchallenged tissues of plants and exogenous applications result in the induction of pathogenesis related (PR) genes and enhanced resistance to a broad range of pathogens. By contrast, JA and ET are usually associated with defence against necrotrophic pathogens and herbivorous insects. Although, SA and JA/ET defence pathways are mutually antagonistic, evidences of synergistic interactions have also been reported (Schenk et al. 2000; Kunkel and Brooks 2002; Beckers and Spoel 2006; Mur et al. 2006). This suggests that the defence signaling network activated and utilized by the plant is dependent on the nature of the pathogen and its mode of pathogenicity. In addition, the lifestyles of different pathogens are not often readily classifiable as purely biotrophic or necrotrophic. Therefore, the positive or negative cross talk between SA and JA/ET pathways may be regulated depending on the specific pathogen (Adie et al. 2007). However, in natural environments, plants often cope with multiple attackers and therefore plants employ complex regulatory mechanisms to trigger effective defence responses against various pathogens and pests. How plants prioritize one response over the other is not known, however. Although JAs are involved in diverse processes such as seed germination, root growth, tuber formation, tendril coiling, fruit ripening, leaf senescence and stomatal opening, they play crucial roles in plant defence responses against insects and microbial pathogens. Several studies have demonstrated that concentrations of JA increase locally in response to pathogen infection or tissue damage and exogenous application of JA induced the expression of defencerelated genes (Lorenzo and Solano 2005; Wasternack 2007). Over the past decade, several mutants affected in JA signal perception and transduction have been isolated and characterised. Three main JA-signaling components include—coronatine insensitive 1 (COI1), jasmonate resistant 1 (JAR1) and Jasmonate insensitive 1/MYC2 (JIN1/MYC2) (Fig. 1). COI1 encodes an F-box protein involved in the SCF-mediated protein degradation by the 26S proteasome and is required for most JA-mediated responses (Xie et al. 1998). JAR1 encodes a JA amino acid synthetase involved in the conjugation of isoleucine to JA (JA-Ile) which is considered to be the bioactive JA molecule perceived by plants (Staswick and Tiryaki 2004; Thines et al. 2007). JIN1/MYC2 encodes a transcription factor involved in the transcriptional regulation of some JA responsive gene expression (Lorenzo et al. 2004).
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Fig. 1 An overview of major components involved in different plant hormone signaling after biotic stress in plants. Biotic stress results in changes in different phytohormone levels. Alterations in plant hormone levels results in the changes in the expression of defence related genes and activation of defence responses. Major components involved in different hormone perception and signaling are shown. A plus (?) sign indicates positive interaction whereas a minus (-) sign indicates negative interaction. See text for further details and abbreviations. (Abbreviations: ABA, abscisic acid; ARFs, Auxin response factors; Aux/IAA, Auxin/Indole-3 acetic acid; BR, brassinosteroid; BRI1, BR insensitive 1; BAK1, BRI1-associated kinase1; BIN2, BR insensitive 2; BRZ1, brassinazole resistant 1; BES1, BRI1 ems suppressor 1; CK, cytokinin; ERF, ethylene response factor; ET, ethylene; GA, gibberellin; GID1, gibberellin insensitive dwarf1; JA, jasmonates; SA, salicylic acid; TFs, transcription factors; TIR1, transport inhibitor response 1)
The recent discovery of jasmonate ZIM-domain (JAZ) proteins has advanced our understanding of the molecular mechanisms of JA signaling in plants. It has been reported that COI1 or COI1-JAZ complex acts as a receptor for JAIle in Arabidopsis (Katsir et al. 2008). JAZ proteins are repressors of JA signaling which have been shown (JAZ1 and JAZ3) to interact with JIN1/MYC2 and inhibit the expression of JA-responsive genes. JA (more specifically JA-Ile) promotes interaction between JAZ proteins and the SCFCOI1 ubiquitin ligase, leading to the ubiquitination and subsequent degradation of JAZ proteins by the 26S proteasome. The degradation of JAZ proteins allows transcription factors (such as MYC2) to activate the expression of JA-responsive genes (Chini et al. 2007; Thines et al. 2007). It is interesting to note that JAZ genes are induced by JA. In addition, myc2 mutants are defective in some but not all JA responses. Recently, JA signaling has been implicated in the long-distance information transmission leading to systemic immunity in Arabidopsis (Truman et al. 2007). Rapid accumulation of JA in phloem exudates of leaves challenged with an avirulent strain of Pst and increased accumulation of JA biosynthetic gene transcripts as well as JA levels in systemic leaves suggests that JA could act as a mobile signal in Arabidopsis
pathogen immunity (Truman et al. 2007). However, Chaturvedi et al. (2008) demonstrate that the mobile signal in SAR is likely to be jasmonates and not JA itself. JA signaling plays a prominent role in promoting plant defence responses to many herbivores including caterpillars, beetles, thrips, leafhoppers, spider mites, fungal gnats and mired bugs (Browse and Howe 2008). For example, JA signaling is activated in response to attack by Manduca sexta caterpillars in tobacco (Kahl et al. 2000), spider mite Tetranychus urticae in tomato (Li et al. 2002a) and Pieris rapae caterpillars or Frankliniella occidentalis thrips in Arabidopsis (Reymond et al. 2004; De Vos et al. 2005). However, not all herbivores activate JA signaling in plants. The silverleaf whitefly Bemisia tabaci activates SA signaling and suppresses JA signaling in Arabidopsis (Kempema et al. 2007) indicating that SA and other hormones are also important for the resistance of plants against some herbivores. However, compared to JAs, the contribution of other phytohormones to host resistance against herbivores appears to be relatively minor (Bodenhausen and Reymond 2007; Koornneef and Pieterse 2008; Zheng and Dicke 2008). Treatment of plants with JA results in enhanced resistance to herbivore challenge (Howe and Jander 2008). Moreover, mutants defective in the biosynthesis or perception of JA show compromised resistance to herbivore attackers (Paschold et al. 2007; Zarate et al. 2007). These results indicate that JA plays a dominant and conserved role in plant resistance to herbivore attack. Interaction between defence signaling pathways is an important mechanism for regulating defence responses against various types of pathogens. In the recent years, several components regulating the cross-talk between SA, JA and ET pathways have been identified. However, the underlying molecular mechanisms are not well understood. Some of the important components mediating the crosstalk between defence signaling pathways are described below.
Interactions between SA, JA and ET signaling pathways SA and JA/ET One of the important regulatory components of SA signaling is non-expressor of PR genes 1 (NPR1), which interacts with TGA transcription factors that are involved in the activation of SA-responsive PR genes (Fig. 1, Dong 2004). Arabidopsis npr1 plants are compromised in the SA-mediated suppression of JA responsive gene expression indicating that NPR1 plays an important role in SA-JA interaction (Spoel et al. 2007). Downstream of NPR1,
several WRKY transcription factors play important roles in the regulation of SA-dependent defence responses in plants (Wang et al. 2006; Eulgem and Somssich 2007). The Arabidopsis WRKY70 has been found to regulate the antagonistic interaction between SA- and JA-mediated defences. Overexpression of WRKY70 resulted in the constitutive expression of SA-responsive PR genes and enhanced resistance to the biotrophic pathogen Erysiphe cichoracearum but repressed the expression of JAresponsive marker gene PDF1.2 and compromised resistance to the necrotrophic pathogen Alternaria brassicicola (A. brassicicola) (Li et al. 2004, 2006). In contrast, suppression of WRKY70 expression caused an increase in PDF1.2 transcript levels and enhanced resistance to A. brassicicola (Li et al. 2006). These results suggest that WRKY70 acts as a positive regulator of SA-dependent defences and a negative regulator of JA-dependent defences and plays a pivotal role in determining the balance between these two pathways. Recently, WRKY62 has been reported to be induced by MeJA and SA synergistically. In addition, the analysis of loss and gain of function mutants in Arabidopsis plants revealed that WRKY62 downregulates JA-responsive LOX2 and VSP2 genes. These results suggest potential involvement of WRKY62 in the SAmediated suppression of JA-responsive defence in Arabidopsis (Mao et al. 2007). Mitogen activated protein kinase 4 (MPK4) has been identified as another key component involved in mediating the antagonism between SA- and JA-mediated signaling in Arabidopsis. The Arabidopsis mpk4 mutants show elevated SA levels, constitutive expression of SA responsive PR genes and increased resistance to Pst. In contrast, the expression of JA responsive genes and the resistance to A. brassicicola were found to be impaired in mpk4 mutants (Petersen et al. 2000; Brodersen et al. 2006). These results indicate that MPK4 acts as a negative regulator of SA signaling and positive regulator of JA signaling in Arabidopsis. Another important regulator identified to affect antagonism between SA and JA mediated signaling is a glutaredoxin, GRX480. Glutaredoxins are disulfide reductases which catalyze thiol disulfide reductions and are involved in the redox regulation of protein activities involved in a variety of cellular processes (Meyer et al. 2008). Recently, GRX480 has been shown to interact with TGA transcription factors involved in the regulation of SA responsive PR genes (Ndamukong et al. 2007). The expression of GRX480 is induced by SA and requires TGA transcription factors and NPR1. Furthermore, the expression of JA responsive PDF1.2 gene was inhibited by GRX480 (Ndamukong et al. 2007). These findings suggest that SA-induced NPR1 activates GRX480, which forms a complex with TGA factors and suppresses the expression of JA-responsive genes.
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A recent identification of a senescence specific transcription factor WRKY53 represents an additional component involved in mediating the cross-talk between SA and JA signaling (Miao and Zentgraf 2007). WRKY53 has been shown to interact with the JA-inducible protein epithiospecifying senescence regulator (ESR). More importantly, the expression of these genes is antagonistically regulated in response to JA and SA suggesting that WRKY53 and ESR mediate negative cross-talk between pathogen resistance and senescence in Arabidopsis (Miao and Zentgraf 2007). The JA-responsive transcription factor JIN1/MYC2 acts as a negative regulator of SA signaling during Pst DC3000 infection in Arabidopsis. The jin1 mutant plants showed increased accumulation of SA, enhanced expression of PR genes and increased resistance to Pst DC3000 compared to the wild type plants (LaurieBerry et al. 2006). JA and ET Several studies indicate that JA- and ET-signaling often operate synergistically to activate the expression of some defence related genes after pathogen inoculation (Penninckx et al. 1998; Thomma et al. 2001; Glazebrook 2005). Microarray analysis of defence related genes revealed significant overlap in the number of genes induced by both JA and ET (Schenk et al. 2000). Furthermore, the induction of PDF1.2 gene by A. brassicicola was found to be inhibited in both jasmonate insensitive mutant coi1 and ethylene insensitive mutant ein2 (Penninckx et al. 1998; Thomma et al. 2001). The Arabidopsis cev1 mutant, that is defective in the cellulose synthase gene CesA3, displays constitutively active JA and ET responses indicating that CEV1 acts as a negative regulator of JA and ET signaling in Arabidopsis (Ellis et al. 2002). It has been shown that an Arabidopsis transcription factor, ethylene response factor 1 (ERF1) acts as a positive regulator of JA and ET signaling (Lorenzo et al. 2003). Recently, several members of ERF family have been shown to play important role in mediating defence responses in Arabidopsis (McGrath et al. 2005). The Arabidopsis transcription factor MYC2 has also been shown to regulate the interaction between JA and ET mediated defence signaling. However, MYC2 induces JA mediated expression of wound response genes but represses the expression of pathogen responsive genes. This indicates that MYC2 differentially regulates JA-responsive pathogen defence and wound response genes in Arabidopsis (Lorenzo and Solano 2005; Dombrecht et al. 2007). It is becoming evident that plants modulate the relative abundance of SA, JA and ET levels, modify the expression of defence-related genes and coordinate complex interactions between defence signaling pathways to activate an effective defence response against attack by various types
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of pathogens and pests. However, how plants coordinate these complex interactions and what are the molecular mechanisms involved is not clear. Identification of molecular players involved in the complex interactions and fine-tuning the balance between different signaling pathways will broaden our understanding of hormone-mediated defence signaling network in plants.
Auxin Auxin promotes the degradation of a family of transcriptional repressors called Auxin/Indole-3-acetic acid (Aux/ IAA). Aux/IAA proteins bind to auxin response factors (ARFs) and inhibit the transcription of specific auxin response genes (Fig. 1, Leyser 2006). It has been shown that transport inhibitor response 1 (TIR1) is an auxin receptor that interacts with Aux/IAA proteins (Kepinski and Leyser 2005; Dharmasiri et al. 2005). TIR1 encodes an F-box protein that forms an Aux/IAA-SCFTIR1 (SKP1, Cullin and F-box proteins) complex and leads to the degradation of Aux/IAA proteins via ubiquitin/26S proteasome pathway (Parry and Estelle 2006). To regulate plant growth and development, auxin can induce the expression of three groups of genes: Aux/IAA family, GH3 family and small auxin-up RNA (SAUR) family (Woodward and Bartel 2005). GH3 genes encode IAA-amido synthetases that are involved in the regulation of auxin homeostasis by conjugating excess IAA to amino acids (Staswick et al. 2005). Most of the total auxin in plants is found in the conjugated form and the formation of auxin conjugates is one of the important regulatory mechanisms for the activation or inactivation of IAA. Auxin responsive GH3 genes have been shown to play roles in plant defence responses in Arabidopsis and Rice. Recently, it has been shown that GH3.5 acts as a bifunctional modulator in both SA and auxin signaling during pathogen infection (Zhang et al. 2007). Similarly, Ding et al. (2008) reported that over expression of GH3-8 resulted in enhanced resistance to the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo), which causes bacterial blight disease in rice, and this resistance was shown to be independent of SA and JA signaling. In addition, GH3-8 over expressing rice plants accumulated higher levels of conjugated IAA (IAA-Asp) and reduced levels of free IAA compared to wild type plants. Interestingly, infection of rice plants with Xoo induced the expression of several IAA biosynthetic genes and resulted in increased accumulation of free IAA. Moreover, GH3-8 over expressing plants showed reduced expression of SA and JA responsive genes as well as reduction in the levels of SA and JA compared to wild type plants (Ding et al. 2008). These findings suggest that GH3-8 mediated resistance to
Xoo in rice is independent of SA and JA pathways. Xooinduced auxin production activates the expression of expansins that result in the loosening of the cell wall and thus could potentiate pathogen growth. This is supported by the observation that the expression of expansin genes was suppressed in the Xoo resistant GH3-8 over expressors (Ding et al. 2008). These results suggest that inhibition of expansin expression by suppressing auxin signaling might act as a physical barrier to restrict Xoo infection in rice. Treatment of Arabidopsis plants with an SA analog, benzothiadiazole S-methyl ester (BTH) resulted in the repression of a number of auxin responsive genes. These genes included an auxin importer AUX1, an auxin exporter PIN7, auxin receptors TIR1 and AFB1, and genes belonging to auxin inducible SAUR and Aux/IAA family (Wang et al. 2007). Similarly, it was found that majority of the above auxin inducible genes were also repressed in systemic tissues after induction of SAR. This indicates that SAR response involves down regulation of auxin responsive genes. However, the level of free auxin did not change after SA treatment. In addition, SA has been shown to inhibit the expression of an auxin inducible reporter DR5::GUS. Wang et al. (2007) argue that SA stabilizes Aux/IAA auxin repressors by limiting auxin receptors that are needed for the down regulation of Aux/IAA proteins. Exogenous application of auxin has been shown to promote disease caused by Agrobacterium tumefaciens (Yamada 1993), Pseudomonas savastanoi (Yamada 1993) and Pst DC3000 (Navarro et al. 2006; Chen et al. 2007). Similarly, co-inoculation of P. syringae pv. maculicola (Psm) 4326 and auxin has been found to promote both disease symptom and pathogen growth in Arabidopsis (Wang et al. 2007). These results indicate that auxin is involved in the attenuation of defence responses in plants. In contrast, blocking auxin responses has been shown to increase resistance in plants. Auxin resistant axr2-1 mutants of Arabidopsis showed reduction in Psm 4326 growth compared to wild type plants (Wang et al. 2007). Several studies have shown that pathogen infection results in imbalances in auxin levels as well as changes in the expression of genes involved in auxin signaling. For example, infection with Pst DC3000 resulted in increased IAA levels in Arabidopsis (O’Donnell et al. 2003). Interestingly, the bacterial type III effector avrRpt2, which encodes a cysteine protease, has been shown to modulate host auxin physiology to promote pathogen virulence and disease development in Arabidopsis (Chen et al. 2007). Global gene expression analysis using microarrays revealed that Pst DC3000 induces auxin biosynthetic genes and represses genes belonging to Aux/IAA family and auxin transporters. Thus, Pst DC3000 activates auxin production, alters auxin movement and derepresses auxin signaling thereby modulating auxin physiology in
Arabidopsis (Thilmony et al. 2006). This suggests that auxin promotes disease susceptibility and repression of auxin signaling could potentially result in enhanced resistance in plants. Indeed, down regulation of auxin signaling has been shown to contribute to plant induced immune responses in Arabidopsis. Navarro et al. (2006) showed that down regulation of auxin receptor genes by over expression of a micro RNA (miR393), which targets auxin receptors, increased resistance against Pst DC3000 in Arabidopsis. In contrast, activation of auxin signaling through over expression of an auxin receptor that is partially refractory to miR393-mediated transcript cleavage, enhanced susceptibility to Pst DC3000 (Navarro et al. 2006). These results suggest that auxin promotes susceptibility to bacterial disease, and that down-regulation of auxin signaling is part of the plant induced immune response. Recently, Llorente et al. (2008) reported that repression of auxin signaling either through mutations in the auxin signaling components or interference with auxin transport compromises resistance of Arabidopsis plants to the necrotrophic fungi Plectosphaerella cucumerina (P. cucumerina) and Botrytis cinerea (B. cinerea). Moreover, infection of virulent necrotrophs such as P. cucumerina results in the down regulation of auxin response genes in Arabidopsis (Llorente et al. 2008). This suggests that auxin signaling is an important component involved in modulating plant responses to necrotrophic fungi. However, the expression of marker genes of SA- and JA-signaling pathways was not impaired in auxin signaling mutants upon P. cucumerina infection. This indicates that the susceptibility of auxin signaling mutants to necrotrophic fungi is not dependent on SA- or JA-mediated defence pathways. Viral pathogens also manipulate auxin signaling components to promote virulence and cause disease. For example, the interactions of tobacco mosaic virus (TMV) replicase with Aux/IAA proteins affect the transcriptional activation of auxin-responsive genes and promote the development of disease symptoms in Arabidopsis and tomato (Padmanabhan et al. 2005, 2006, 2008). Furthermore, the TMV replicase was shown to interact with and disrupt the nuclear localization of several related Arabidopsis Aux/IAA proteins (Padmanabhan et al. 2006). This indicates that TMV could disrupt Aux/IAA functions as a means to reprogram the cellular environment for virus replication and spread (Padmanabhan et al. 2008). Taken together, emerging evidence suggests that auxin acts as an important component of hormone signaling network involved in the regulation of defence responses against various biotrophic and necrotrophic pathogens. Auxin regulates the expression of genes associated with the biosynthesis, catabolism and signaling pathways of other hormones (Paponov et al. 2008) and modulates defence
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and development responses. However, how auxin levels affect the balance of other hormones and fine tune defence responses specific to different pathogens remains to be discovered.
Abscisic acid ABA is involved in the regulation of many aspects of plant growth and development including seed germination, embryo maturation, leaf senescence, stomatal aperture and adaptation to environmental stresses (Wasilewskaa et al. 2008). Several recent papers have reported that ABA plays important roles in plant defence responses (Mauch-Mani and Mauch 2005; Mohr and Cahill 2007; de Torres-Zabala et al. 2007; Adie et al. 2007). However, the role of ABA in plant defence appears to be more complex, and vary among different types of plant-pathogen interactions. In general, ABA is shown to be involved in the negative regulation of plant defence against various biotrophic and necrotrophic pathogens. For example, the ABA-deficient sitiens mutant of tomato showed more resistance to B. cinerea (Audenaert et al. 2002), Pst (Thaler and Bostock 2004), Oidium neolycopersici (Achuo et al. 2006) and Erwinia chrysanthemi (Asselbergh et al. 2008) than wild type plants. Similarly, the ABA-deficient aba2-1 mutant of Arabidopsis showed more resistance to Fusarium oxysporum (Anderson et al. 2004) and the aba1-1 mutant showed less susceptibility to Hyaloperonospora arabidopsidis (Mohr and Cahill 2003) compared to wild type plants. The Arabidopsis mutants impaired in ABA biosynthesis or sensitivity show more resistance to Pst DC3000 (de TorresZabala et al. 2007) and B. cinerea (Adie et al. 2007). Likewise, exogenous application of ABA enhances susceptibility of various plant species to bacterial and fungal pathogens. For example, application of ABA enhanced the susceptibility of Arabidopsis plants to Pst (de TorresZabala et al. 2007), soybean plants to Phytophthora sojae (Mohr and Cahill 2001) and rice plants to Magnaporthe grisea (Koga et al. 2004). Recently, Yasuda et al. (2008) reported that ABA treatment suppressed SAR induction indicating that there is an antagonistic interaction between SAR and ABA signaling in Arabidopsis. Taken together, these results suggest that ABA acts as a negative regulator of defence responses in various plant pathosystems. However, the role of ABA as a positive regulator of defence has also been reported (Mauch-Mani and Mauch 2005). ABA activates stomatal closure that acts as a barrier against bacterial infection (Melotto et al. 2006). As a result, ABA deficient mutants show more susceptibility to Pst. In addition, treatment with ABA protects plants against A. brassicicola and P. cucumerina indicating that ABA acts as a positive signal for defence against some
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necrotrophs (Ton and Mauch-Mani 2004). In contrast, mutants deficient in ABA are more sensitive to infection by the fungal pathogens A. brassicicola, Pythium irregulare (P. irregulare) (Adie et al. 2007) and Leptosphaeria maculans (Kaliff et al. 2007). These results demonstrate that ABA is not a positive regulator of plant defence against all necrotrophs and its role depends on individual plant pathogen interactions. Pathogen challenge results in the alteration of ABA levels in plants. For example, tobacco plants infected with TMV showed increased ABA levels and treatment with ABA enhanced TMV resistance in tobacco (Whenham et al. 1986). Similarly, Arabidopsis plants challenged with Pst DC3000 accumulated higher levels of ABA and JA compared to unchallenged plants (de Torres-Zabala et al. 2007). These data suggest that some pathogens might have evolved abilities to produce ABA or ABA-mimic to interfere with the host defence. Interestingly, in planta expression of the bacterial type III effector, AvrPtoB, increases foliar ABA and JA levels in Arabidopsis (de Torres-Zabala et al. 2007). However, changes in ABA levels are relatively moderate compared to the changes in the levels of SA, JA or ET after pathogen challenge (Mauch-Mani and Mauch 2005). Moreover, there is a strong similarity between the transcripts induced by ABA and bacterial type III effectors in Arabidopsis. Genome wide expression analyses have revealed the existence of a significant (42%) overlap in the expression of genes regulated by ABA and bacterial type III effectors in Arabidopsis (de Torres-Zabala et al. 2007). Similarly, meta analysis of pathogen inducible genes in Arabidopsis showed that approximately one-third of the ABA-regulated genes are induced by P. irregulare infection (Adie et al. 2007). This indicates that ABA plays an important role in the activation of plant defence through transcriptional reprogramming of plant cell metabolism. Moreover, Adie et al. (2007) also demonstrated that ABA is required for JA biosynthesis and the expression of JA responsive genes after P. irregulare infection. How ABA modulates plant defence responses? ABA has been shown to induce resistance partly through priming the deposition of callose (Flors et al. 2008). Hernandez-Blanco et al. (2007) provide evidence for a direct involvement of ABA signaling in the control of Arabidopsis resistance to R. solanacearum. Arabidopsis mutants affected in cellulose synthase genes required for secondary cell-wall formation show increased induction of ABA-responsive defence-related genes. This suggests that ABA could exert its effect on plant defence by modulating cell wall metabolism in Arabidopsis. Recently, it has been shown that ABA induced the expression of a catalase (CAT1), a scavenger of H2O2, and at the same time activated H2O2 production. ABA-induced CAT1 expression and H2O2
production is mediated by AtMKK1- and AtMPK6-coupled MAPK signaling cascades (Xing et al. 2008). Moreover, H2O2 treatment induced the expression of CAT1 in a concentration-dependent manner (Xing et al. 2008). This suggests that H2O2 might be involved in ABAinduced CAT1 expression and CAT1 is probably involved in its feedback regulation of the H2O2 signaling apart from its ROS scavenging function. Accumulating evidence suggests that ABA regulates defence responses through its effects on callose deposition, production of reactive oxygen intermediates and regulation of defence gene expression. However, the exact molecular mechanism of ABA action on plant defence responses against diverse pathogens remains unclear. Since ABA is involved in both biotic and abiotic stress signaling, the cross-talk between these signaling pathways and the molecular mechanisms involved remain obscure. Dissecting key factors involved in ABA mediated cross-talk between biotic and abiotic stress signaling merits extensive future study.
Gibberellin Gibberellin (GA) was originally identified as a substance secreted from the fungus Gibberella fujikuroi, which causes ‘bakanae’ (or foolish seedling) disease in rice (Kurosawa 1926). GA promotes plant growth by stimulating degradation of negative regulators of growth called DELLA proteins. The rice GA receptor gibberellin insensitive dwarf1 (GID1) interacts with the rice DELLA protein slender rice1 (SLR1) in a GA-dependent manner (Fig. 1). The binding of GID1 to DELLA results in ubiquitination and degradation of DELLA via a ubiquitin E3 ligase SCF complex and the 26S proteasome (UeguchiTanaka et al. 2005; Griffiths et al. 2006). GAs are produced not only by higher plants, but also by fungi and bacteria (MacMillan 2001). It is supposed that GAs in fungi and bacteria are secondary metabolites that act as signaling factors to establish the interaction with host plants. GA has received little attention in the elucidation of signaling components involved in defence responses. However, emerging evidence suggests that GA signaling components play major roles in plant disease resistance and susceptibility. Recently, it has been found that Arabidopsis DELLA proteins, which act as negative regulators of GA signaling, control plant immune responses by modulating SA and JA dependent defence responses (Navarro et al. 2008). The Arabidopsis quadruple-della mutant that lacks four DELLA genes (gai-t6, rga-t2, rgl1-1, rgl2-1) is very susceptible to the fungal necrotrophic pathogens A. brassicicola and B. cinerea, but more resistant to biotrophic pathogens Pst DC3000 and Hyaloperonospora arabidopsidis (Navarro
et al. 2008). Furthermore, Pst DC3000-challenged quadruple-della mutants showed earlier and stronger induction of SA marker genes PR-1 and PR-2 whereas the expression of JA/ET marker gene PDF1.2 (Plant defensin 1.2) was significantly delayed in the quadruple-della mutants compared to Pst DC3000 challenged wild type plants. In contrast, DELLA over accumulating mutants, such as ga1-3, gai and sly1-10, were more resistant to A. brassicicola and more susceptible to Pst DC3000. These results suggest that DELLA proteins promote resistance to necrotrophs by activating JA/ET-dependent defence responses but susceptibility to biotrophs by repressing SA-dependent defence responses in Arabidopsis. Thus, DELLA proteins appear to integrate plant defence response pathways involving SA and JA/ET. DELLA proteins have also been shown to integrate responses to independent hormonal and environmental signals of adverse conditions (Achard et al. 2006). Since GA stimulates degradation of DELLA proteins, it is likely that GA promotes resistance to biotrophs and susceptibility to nectrotrophs. In support of this hypothesis, exogenous application of GA resulted in enhanced resistance to Pst DC3000 and susceptibility to A. brassicicola in Arabidopsis indicating that GA acts as a virulence factor for necrotrophic pathogens. These results suggest that Gibberella might secrete GA as a virulence factor to promote the degradation of DELLA proteins and attenuate JA-dependent defence responses resulting in the loss of DELLA-mediated growth restraint. How DELLA proteins regulate defence responses against various biotrophic and necrotrophic pathogens? Recently, it has been shown that DELLA proteins promote the expression of genes encoding ROS detoxification enzymes thereby regulating the levels of ROS after biotic or abiotic stress (Achard et al. 2008). In consistence with this, della penta mutants (that lack all five DELLA genes) accumulate higher levels of ROS after biotic stress and show down regulation of ROS detoxification enzymes compared to wild type plants (Bari and Jones, unpublished results). Thus, it seems that DELLA proteins regulate plant defence responses against various biotrophic and necrotrophic pathogens at least in part through the modulation of ROS levels in plants. How DELLA proteins regulate the expression of ROS detoxification enzymes and how DELLA-mediated modulation of ROS levels act as biological signals to regulate plant growth and stress responses remains unclear. Mutants affected in GA perception have been shown to affect defence responses in plant. It has been demonstrated that gid1 mutant of rice, defective in GA receptor, accumulates higher GA levels and shows enhanced resistance to the blast fungus Magnaporthe grisea compared to wild type plants (Tanaka et al. 2006). In addition, the expression of a GA inducible protein PBZ1 (probenazole inducible 1)
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was found to be elevated in gid1 mutants. Probenazole is a fungicide which is effective against blast disease in rice (Midoh and Iwata 1996). Furthermore, the expression of PBZ1 is induced by rice blast infection. Since, gid1 mutants accumulate high amounts of GA, PBZ1, and show increased resistance to the blast fungus, the accumulation of PBZ1 appears to play important role in resistance against blast in rice. This indicates that GA signaling components play roles in defence signaling in rice (Tanaka et al. 2006). Modulation of bioactive GA levels through GA deactivating enzymes has been shown to affect disease resistance in plants. Recently, Yang et al. (2008) reported that a GA deactivating enzyme called Elongated Uppermost Internode (EUI) regulates bioactive GA levels and is involved in disease resistance against bacterial and fungal pathogens in rice. The loss of function eui mutants accumulate high levels of GAs and show compromised resistance whereas EUI overexpressors accumulate low levels of GAs and show increased resistance to Xoo and M. oryzae in rice (Yang et al. 2008). Consistent with this, eui plants treated with a GA biosynthesis inhibitor, uniconazole, restored resistance whereas exogenous application of GA to EUI overexpressors compromised resistance to Xoo. These results indicate that GA plays a negative role in basal disease resistance in rice. Viral proteins have also been shown to affect GA signaling components in plants. For example, expression of a GA biosynthetic enzyme, ent-kaurene oxidase, was repressed in rice plants infected with rice dwarf virus (RDV) resulting in a dwarf phenotype (Zhu et al. 2005). It has been shown that P2 protein of RDV interacts with rice ent-kaurene oxidases and affects the production of GA. RDV infected rice plants showed significant reduction in GA level and treatment of infected plants with GA restored normal growth phenotype (Zhu et al. 2005). Infection of rice plants with RDV results in stunting and dark leaves, symptoms that are characteristic of GA-deficient rice mutants. These observations indicate that RDV modulates GA metabolism to promote disease symptoms in rice. Accumulating evidence indicates that GA and its signaling components play important roles in regulating defence responses against various biotrophic and necrotrophic pathogens. However, the mechanism of GA action on defence responses is largely unknown and several interesting questions remain to be answered. For example, what other GA biosynthesis and signaling components are potential targets of pathogen effectors? How does GA regulate the expression of defence genes and modulate changes in metabolism in response to pathogen attack? Do pathogens modulate GA levels in planta? What is the dynamics of DELLA protein complexes in response to pathogens attack? What are the DELLA downstream
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targets involved in plant immunity? It would be interesting to know how GA modulates the balance of other hormone levels and regulates appropriate defence and developmental responses in plants.
Cytokinin Cytokinins (CK) are plant hormones involved in diverse processes including stem-cell control, vascular differentiation, chloroplast biogenesis, seed development, growth and branching of root, shoot and inflorescence, leaf senescence, nutrient balance and stress tolerance (Muller and Sheen 2007). Although, the role of CK in plant defence is poorly understood, there are indications that CK is involved in the regulation of plant defence responses against some pathogens. CK plays an important role in the development of club root disease caused by Plasmodiophora brassicae in Arabidopsis (Siemens et al. 2006). Global gene expression analysis of P. brassicae infected Arabidopsis resulted in differential expression of more than 1,000 genes compared to control plants. Interestingly, genes involved in cytokinin homeostasis (cytokinin synthases and cytokinin oxidases/dehydrogenases) were strongly downregulated. Transgenic plants overexpressing cytokinin oxidase/dehydrogenase genes showed resistance against P. brassicae infection suggesting that cytokinin acts as a key factor in the development of clubroot disease in Arabidopsis (Siemens et al. 2006). However, the molecular mechanism how CK influences plant defence is not known. Recently, infection with Rhodococcus fascians has been shown to modulate cytokinin metabolism in Arabidopsis (Depuydt et al. 2008). It has been shown that A. tumefaciens modifies CK biosynthesis by sending a key enzyme into plastids of the host plant to promote tumorigenesis (Sakakibara et al. 2005). Constitutive activation of a resistance (R) protein in Arabidopsis has been shown to display morphological defects through the accumulation of CK indicating the involvement of CK pathway in some R protein-mediated responses (Igari et al. 2008).
Brassinosteroids Brassinosteroids (BRs) are a unique class of plant hormones that are structurally related to the animal steroid hormones and involved in the regulation of growth, development and various physiological responses in plants (Bajguz 2007). Although, BRs are known to influence various developmental processes including seed germination, cell division, cell elongation, flowering,
reproductive development, senescence, and abiotic stress responses in plants, very little is known about their role in plant responses to biotic stresses. Emerging evidence indicates that BRs are involved in the regulation of plant defence responses. It has been reported that BR enhances resistance to TMV, Pst and Oidium sp. in tobacco. Similarly, BR was shown to increase the resistance of rice plants against M. grisea and Xanthomonas oryzae infection (Nakashita et al. 2003). However, BR induced resistance does not require SA biosynthesis and activation of PR gene expression indicating that BR mediated resistance is independent of SA mediated defence signaling in plants. Exogenous application of 24-epibrassinolide, a BR, was shown to prevent the development of disease symptoms on tomato plants inoculated with Verticillium dahliae, whereas untreated plants showed moderate to severe disease symptoms (Krishna 2003). Similarly BR sprayed potato plants showed resistance to infection by Phytophthora infestans and this resistance was found to be associated with increases in the levels of ABA and ET (Krishna 2003). This suggests that there is a cross-talk between BR and other hormone signaling in mediating defence responses in plants. Several important components of BR signaling are also involved in the modulation of plant defence responses. Recently, three independent research groups have demonstrated the involvement of a critical component of brassinosteroid signaling, BRI1-associated kinase 1 (BAK1) in the regulation of basal defence and programmed cell death in plants (Chinchilla et al. 2007; Kemmerling et al. 2007; Heese et al. 2007). BAK1 is known to interact with the BR receptor, BRI1, and mediate BR signal transduction in plants (Li et al. 2002b; Nam and Li 2002). BAK1 (also known as SERK3, somatic embryogenesis-related kinase 3) is up regulated in response to PAMPs (such as flg22 and elf18) and mutant bak1 plants in Arabidopsis are compromised in PAMP responses as evidenced by loss of ROS burst and growth inhibition in response to flg22 (Chinchilla et al. 2007; Heese et al. 2007). Interestingly, bak1 mutants developed spreading necrosis upon pathogen infection. Furthermore, bak1 mutants showed enhanced susceptibility to necrotrophic pathogens such as A. brassicicola and B. cinerea, whereas resistance to biotrophic pathogen H. parasitica was enhanced in the mutant compared to wild type plants (Kemmerling et al. 2007). Moreover, exogenous BR application failed to restore resistance to fungal pathogens and mutants affected in other BR signaling components did not show enhanced susceptibility to the above fungal pathogens (Kemmerling et al. 2007). Heese et al. identified the Nicotiana benthamiana homolog of BAK1 and found that knockdown of the protein in this plant allowed enhanced growth of bacteria on the
plants. These findings suggest that BAK1 plays a BRindependent role in regulating cell death in Arabidopsis. Another related protein BAK1-like 1 (BKK1) has been shown to function redundantly with BAK1 and is involved in the positive regulation of BR dependent plant growth pathway and negative regulation of BR-independent cell-death pathway in Arabidopsis (He et al. 2007). Interestingly, BAK1 has been found to interact with the flagellin receptor, FLS2, in a ligand-dependent manner (Chinchilla et al. 2007; Heese et al. 2007). These data suggest a model where binding of flagellin to FLS2 promotes the formation of an active complex with BAK1 which results in the activation of downstream signaling components. However, the function of BAK1 in plant defence is BR-independent suggesting that BAK1 has dual role in the regulation of plant defence and development. Recently, Shan et al. (2008) demonstrated that bacterial effectors, AvrPto and AvrPtoB, target BAK1 and prevent the flagellin induced FLS2-BAK1 interaction, thereby impeding the initiation of PAMP-signaling. This indicates that BAK1 is an important regulator of PAMPsignaling and it is possible that BAK1 interacts with other unknown PRRs which might be targets for bacterial effectors. It has been shown that beet curly top virus (BCTV) C4 functionally interacts with brassinosteroid insensitive 2 (BIN2), a glycogen synthase kinase 3-like (GSK3-like) protein kinase involved in brassinosteroid signaling in Arabidopsis (Piroux et al. 2007). BIN2 is one of the 10 GSK3-like kinases in Arabidopsis (Jonak and Hirt 2002) and is considered to be a negative regulator of the brassinosteroid signal transduction pathway (Li and Nam 2002). It has been demonstrated that BIN2 phosphorylates transcription factors BRI1-ems-suppressor 1 (BES1) and brassinazole-resistant 1 (BZR1) and targets them for degradation by the proteasome (Li and Nam 2002). It appears that binding of BCTV viral protein C4 to BIN2 subverts brassinosteroid signaling by downregulating BIN2 activity and activating the transcription of BES1 and BZR1 responsive genes (Piroux et al. 2007). BR has also been reported to affect the expression of genes involved in defence as well as biosynthesis of other hormones. For example genes involved in biosynthesis of ET (ACC synthase) and JA (OPR3) in Arabidopsis, were induced by BR (Yi et al. 1999; Muessig et al. 2006). Whether JA or ET is required for BR induced resistance is not known. Collectively, these results indicate that BRs and its signaling components are involved in the modulation of plant defence responses against various pathogens. However, our knowledge on the role of BR on plant defence has started to emerge and the molecular mechanisms involved remains to be understood.
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Peptide hormones Peptide hormones comprise a new class of hormones and are involved in the regulation of various aspects of plant growth and development including defence responses against attacking pathogens and pests (Matsubayashi and Sakagami 2006; Farrokhi et al. 2008). The peptide hormones are usually processed from larger polypeptide precursors. Examples of plant peptide hormones include systemin, hydroxyproline-rich glycopeptides, AtPep1, CLAVATA3, PHYTOSULFOKINE, POLARIS, ROTUNDIFOLIA4/DEVIL1, inflorescence deficient in abscission gene (IDA), early nodulin 40 (ENOD40), nodule specific cysteine-rich (NCR), and S-locus cysteine-rich protein (SCR). Defence-related peptide hormones include systemin (Pearce et al. 1991), hydroxyproline-rich glycopeptide systemins (Pearce et al. 2001, 2007; Pearce and Ryan 2003) from solanaceous plants and AtPep1 peptide from Arabidopsis (Huffaker et al. 2006). These peptides are from 18 to 23 amino acids in length, are processed from wound- and JA-inducible precursor proteins, and play roles in the activation of local and systemic responses against wounding and pest attack. Systemin is synthesized from prosystemin and stored in the cytoplasm (Narvaez-Vasquez and Ryan 2004). In contrast, hydroxyproline-rich glycopeptide systemins are processed from precursors that are synthesized through the secretory pathway and localized in the cell walls (Narvaez-Vasquez et al. 2005). Initially, systemin was considered to be the systemic signal responsible for the activation of systemic defence responses against wounding and herbivore attack (Pearce et al. 1991; McGurl et al. 1992). However, recent grafting experiments with JA biosynthetic and perception mutants indicate that the systemic signal is likely to be derived from the octadecanoid pathway but not necessarily JA itself (Li et al. 2002c; Lee and Howe 2003) because neither JA nor systemin is needed in the systemic, undamaged leaves of tomato plants. This suggests that systemin acts at or near the site of wounding by inducing and amplifying the JA-derived mobile signal and activates the systemic response (Schilmiller and Howe 2005). Systemin regulates the expression of several genes involved in the octadecanoid pathway and herbivore defence in tomato (Ryan 2000). Tomato plants overexpressing prosystemin show enhanced resistance whereas plants with reduced systemin levels show more susceptibility to insect herbivory (Orozco-Cardenas et al. 1993). Likewise, overexpression of the tobacco hydroxyprolinerich glycopeptide precursor gene resulted in the activation of proteinase inhibitor genes and increased resistance to feeding by Helicoverpa armigera larvae in tobacco (Ren and Lu 2006). Both systemin and hydroxyproline-rich
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glycopeptides can activate the expression of anti-herbivore proteinase inhibitors and polyphenol oxidase in response to wounding and methyl jasmonate. AtPep1, a 23 amino acid peptide derived from precursor PROPEP1 in Arabidopsis, acts as an elicitor and activates the expression of defence related genes (Huffaker et al. 2006). The gene encoding the precursor can be induced by wounding, methyl jasmonate, ethylene and SA. Constitutive expression of PROPEP1 gene in Arabidopsis results in the constitutive transcription of PDF1.2 and enhanced resistance to P. irregulare (Huffaker and Ryan 2007). These results suggest that defense-signaling peptides play important roles in the activation of defence against invaders probably by amplifying the signal initiated by wounding and elicitors. However, the underlying molecular mechanism involved in the activation of these peptide hormones in regulating plant defence remains elusive.
Conclusions and perspectives Plant hormones regulate complex signaling networks involving developmental processes and plant responses to environmental stresses including biotic and abiotic stresses. Significant progress has been made in identifying the key components and understanding plant hormone signaling (especially SA, JA and ET) and plant defence responses (Fig. 1). Several recent studies provide evidence for the involvement of other hormones such as ABA, auxin, GA, CK and BR in plant defence signaling pathways. Treatment of plants with some hormones results in the reprogramming of the host metabolism, gene expression and modulation of plant defence responses against microbial challenge. Depending on the type of plant–pathogen interactions, different hormones play positive or negative roles against various biotrophic and necrotrophic pathogens (Fig. 2). However, the underlying molecular mechanisms are not well understood and several questions remain to be answered. For example, how is the intracellular level of phytohormones regulated in response to various pathogens? Plant hormone signaling pathways are not isolated but rather interconnected with a complex regulatory network involving various defence signaling pathways and developmental processes. To understand how plants coordinate multiple hormonal components in response to various developmental and environmental cues is a major challenge for the future. It is important to note that the type of interactions and plant responses to stresses vary depending on the pathosystem as well as the time, quantity and the tissue where hormones are produced. Another important question to answer is how different hormone-mediated developmental and defence-related responses are regulated
Fig. 2 A simplified model showing the involvement of different hormones in the positive or negative regulation of plant resistance to various biotrophic and necrotrophic pathogens. The arrows indicate activation or positive interaction and blocked lines indicate repression or negative interaction. See text for further details and abbreviations
in specific tissues and cell types? Most of the studies in understanding phytohormone signaling have been done using seedlings and there is limited study on mature leaves. More studies using mature leaves are necessary to understand the role of hormone signaling components involved in plant defence against various pathogens. In addition to the production of hormones by plants, several plant pathogens also produce phytohormones or their functional mimics to manipulate defence-related regulatory network of plants. Emerging evidence suggests that plant pathogens manipulate components of hormone biosynthesis and signaling machinery leading to hormone imbalances and alterations in plant defence responses. This is one of the strategies used by some pathogens to confer virulence and cause disease. However, we have very limited knowledge on how pathogen effectors confer virulence by modulating hormone signaling components. Recent global expression profiling studies in response to pathogen challenges are providing useful information about different components involved in the complex interactions between hormone-regulated defence signaling pathways. However, additional studies involving mature leaves and detailed time course experiment will be necessary to extend our understanding of the complex regulatory mechanisms operating between plant hormone signaling and plant defence responses. A better understanding of phytohormone-mediated plant defence responses is important in designing effective strategies for engineering crops for disease and pest resistance. Acknowledgements We apologize to our colleagues whose work could not be cited in this review because of space limitations. We thank, Lionel Navarro, Alexandre Robert-Seilaniantz and Georgina Fabro for critical comments. The Sainsbury Lab is funded by the Gatsby Charitable Foundation. R. Bari is funded by a grant from the BBSRC.
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