Jasmonic Acid at the Crossroads of Plant Immunity and Pseudomonas syringae Virulence

Abstract

Sensing of pathogen infection by plants elicits early signals that are transduced to affect defense mechanisms, such as effective blockage of pathogen entry by regulation of stomatal closure, cuticle, or callose deposition, change in water potential, and resource acquisition among many others. Pathogens, on the other hand, interfere with plant physiology and protein functioning to counteract plant defense responses. In plants, hormonal homeostasis and signaling are tightly regulated; thus, the phytohormones are qualified as a major group of signaling molecules controlling the most widely tinkered regulatory networks of defense and counter-defense strategies. Notably, the phytohormone jasmonic acid mediates plant defense responses to a wide array of pathogens. In this review, we present the synopsis on the jasmonic acid metabolism and signaling, and the regulatory roles of this hormone in plant defense against the hemibiotrophic bacterial pathogen Pseudomonas syringae. We also elaborate on how this pathogen releases virulence factors and effectors to gain control over plant jasmonic acid signaling to effectively cause disease. The findings discussed in this review may lead to ideas for the development of crop cultivars with enhanced disease resistance by genetic manipulation.

Keywords: Pseudomonas syringae; effectors; jasmonates; salicylic acid; stomata.

Figure 1

Metabolism of jasmonates (JAs). (a) Jasmonic acid (JA) is synthesized from α-linolenic acid by the various enzymes present in chloroplasts (CPs) and peroxisomes (PRs) [12]. LOX, AOS, and AOC are the key enzymes of JA biosynthesis present in CPs. These enzymes convert α-linolenic acid into OPDA through a series of reactions. OPDA is then exported from the CPs by the JASSY transmembrane protein present on the inner membrane of the CPs [13]. OPDA enters into PRs through an ABC transporter membrane protein known as COMATOSE (CTS) [14]. OPDA is directly converted to JA in the PRs with the help of OPR3 and ACX1 enzymes through β-oxidation, and then transported into the cytoplasm (CM) [12]. In the absence of a functional OPR3 enzyme, OPDA is converted to 4,5-ddh-JA, which is then transported into the CM [18,19]. The 4,5-ddh-JA is now converted to JA through the OPR2 enzyme in the CM. In the CM, JAR1 and JMT act on the JA and convert it into JA-Ile [16] and MeJA [15], respectively. (b) JA catabolism is regulated by CYP94B1, CYP94B3, and CYP94C1 present in the endoplasmic reticulum (ER) and amidohydrolases IAR3 and ILL6 [22]. (i) CYP94B1 and CYP94B3 degrade JA-Ile to the weak analog 12OH-JA-Ile, while CYP94B3 and CYP94C1 catalyze JA-Ile to the inactive form 12COOH-JA-Ile [21,22,23,24,25,26] (i). JA-Ile is also converted to JA with the help of IAR3 and ILL6 enzymes [28] (ii). These enzymes also work downstream to the CYP94s and breakdown 12OH-JA-Ile generated from step (i) to 12OH-JA. In an alternative catabolic route, JOX hydroxylates JA to 12OH-JA [27] (iii). ACXI, ACYL-CoA-OXIDASE 1; AOC, ALLENE OXIDE CYCLASE; AOS, ALLENE OXIDE SYNTHASE; 12COOH-JA-Ile, 12-carboxy-jasmonic acid isoleucine; CYP94, CYTOCHROME P450 MONOOXYGENASE CYP94 FAMILY; 4,5-ddh-JA, 4,5-didehydro-jasmonic acid; dnOPDA; dinor-oxo-phytodienoic acid; 12,13-EOT,12,13-epoxyoctadecatrienoic acid; 13-HPOT, 13-hydroperoxyoctadecatrienoic acid; IAR3, INDOLE ACETIC ACID (IAA)-ALANINE RESISTANT 3; ILL6, IAA-LEUCINE RESISTANT (ILR)-LIKE GENE 6; JA-Ile, isoleucine conjugated jasmonate; JAO, JASMONIC ACID OXIDASE; JAR1, JASMONATE RESISTANT 1; JASSY, a membrane channel that is located in the outer envelope of chloroplasts; JMT, S-ADENOSYL-L-METHIONINE: JASMONIC ACID CARBOXYL METHYLTRANSFERASE; LOX, 13-LIPOXYGENASE; MeJA, methyl jasmonate; 12OH-JA, 12-hydroxy-jasmonic acid; 12OH-JA-Ile, 12-hydroxy-jasmonic acid isoleucine; OPC8, 3-oxo-2(2′[Z]-pentenyl)-cyclopentane-1-octanoic acid; OPDA, 12-oxo-phytodienoic acid; OPR, OPDA REDUCTASE; tnOPDA, tetranor-oxo-phytodienoic acid.

Figure 2

Overview of the jasmonic acid (JA) signaling pathway. (a) In the non-inductive phase of JA signaling or in the absence of jasmonates (JAs), JAZ proteins form a complex with the co-repressor TPL and TPR proteins [31]. The association between JAZs and TPL–TPR co-repressors is mediated by the NINJA adaptor protein [32]. The JAZ^NINJA–TPL–TPR repressor complex then binds to the transcription factors (TFs, such as MYCs, EIN3, and EIL1) and prevents the induction of JA signaling (i). JAZ proteins also recruit the transcriptional co-repressor HDA6 protein, which deacetylates histones (especially H4) and inhibits EIN3 and EIL1 to bind to the target gene promoters, leading to the subsequent repression of JA-responsive gene transcription [34,35] (ii). (b) When a sufficient level of JA-Ile is present in the cells (induction phase), JA-Ile enters into the nucleus through JAT1 membrane transporter [36] and binds to COI1 and JAZ^NINJA–TPL–TPR repressor complex, leading to the COI1-mediated polyubiquitination of JAZ. The polyubiquitination tags JAZ proteins for 26S proteasome-mediated breakdown, thereby releasing the TFs and JA-signaling repressors from the complex. Inositol pentakisphosphate (InsP₅), a co-receptor for JA-Ile, stabilizes the association of COI1–JAZ complex [37]. Depending upon the nature of infecting pathogens, the JA signaling operates through either (i) MYC or (ii) ERF TFs. The regulation of JA signaling in the MYC2 branch involves the association of HAC1 with MYC2 and MED25 proteins and binding of various MYC TFs [38]. This activator complex then induces the transcription of the downstream JA-responsive gene (e.g., VSP2) (i). The regulation of JA signaling through the ERF branch is mediated by ethylene (ET), EIN3, and EIL1. EIN3 and EIL1 TFs induce the transcription of ERF1 and ORA59. ERF1 and ORA59 TFs, in turn, recruit MED25 to the GCC-box motif in the target gene promoters, leading to the activation of JA-responsive genes (e.g., PDF1.2) [39] (ii). Double-headed bars show mutual repression, while dotted arrows indicate the release of TFs from the repressor complex. L-arrows and L-bars indicate induction and repression of gene transcription, respectively. Crosses indicate the inability of proteins to bind to DNA sequences. COI1, CORONATINE INSENSITIVE 1 receptor; EIL1, ETHYLENE-INSENSITIVE 3-LIKE 1; EIN3, ETHYLENE-INSENSITIVE 3; ERF, ETHYLENE RESPONSE FACTOR; GTFs, general transcription factors; HAC1, HISTONE ACETYLTRANSFERASE OF THE CBP FAMILY 1; HDA, HISTONE DEACETYLASE; InsP₅, inositol pentakisphosphate; JA-Ile, isoleucine conjugated jasmonate; JAT1, JASMONATE TRANSPORTER 1; JAZ, JASMONATE ZINC-FINGER EXPRESSED IN INFLORESCENCE MERISTEM (ZIM)-DOMAIN PROTEIN; MED25, a subunit of the MEDIATOR transcriptional co-activator complex; MYC, MYELOCYTOMATOSIS; NINJA, NOVEL INTERACTOR OF JAZ; ORA59, OCTADECANOID-RESPONSIVE ARABIDOPSIS AP2 (APETALA2)/ERF59; PDF1.2, PLANT DEFENSIN 1.2; RNA Pol II, RNA POLYMERASE II; TPL, TOPLESS; TPR, TPL-RELATED proteins; VSP2, VEGETATIVE STORAGE PROTEIN 2.

Figure 3

Negative regulation of the jasmonic acid (JA) signaling in Arabidopsis. (a) JAZs bind to transcription factors (TFs), such as JAM1 and JAM2, and compete with MYC2 for binding to the promoters of JA-responsive genes to repress their transcription [51]. (b) JAZ proteins (e.g., JAZ8) also interact with JASMONATE-ASSOCIATED VQ MOTIF GENE 1 (JAV1) and WRKY51 to form a “JJW” co-repressor complex. The JJW complex, in turn, binds to the promoter of JA-biosynthetic genes (e.g., AOS) and represses their expression, inhibiting JA biosynthesis [53]. (c) MYC2 is polyubiquitinated by PUB10 and is targeted for degradation, while it is stabilized by UBP12- and UBP13-mediated deubiquitination [54,55]. (d) The JA-signaling pathway is subjected to feedback regulation by a CUL3^BPM E3 ligase system. The BPM proteins interact with MYC2, 3, and 4 and associate these proteins with the CUL3 ^BPM E3 ligase complex for ubiquitination and subsequent breakdown. This process leads to the transcription repression of the downstream JA-responsive genes [56]. Bars show repression, and L-bars indicate repression of gene transcription. Cross indicates the inability of proteins to bind to DNA sequences. AOS, ALLENE OXIDE SYNTHASE; BPM, ((BTB/POZ (BROAD COMPLEX, TRAMTRACK, BRIC-A-BRAC/POX VIRUS, AND ZINC FINGER DOMAIN) and MATH (MEPRIN AND TRAF HOMOLOGY DOMAIN)); CUL3, CULIN3; JAM, JA-ASSOCIATED MYC2-LIKE; JAV1, JASMONATE-ASSOCIATED VQ MOTIF GENE 1; JAZ, JASMONATE ZINC-FINGER EXPRESSED IN INFLORESCENCE MERISTEM (ZIM)-DOMAIN PROTEIN; JJW, JAV1, JAZ, WRKY51; MED25, a subunit of the MEDIATOR transcriptional co-activator complex; MYC, MYELOCYTOMATOSIS; PUB10, PLANT U-BOX PROTEIN 10; UBP, UBIQUITIN-SPECIFIC PROTEASE.

Figure 4

A summary of the Pseudomonas syringae factors manipulating jasmonic acid (JA) signaling. Different strains of P. syringae secrete virulence factors or effectors to gain control over the plant JA-signaling pathway. (a) P. syringae pv. tomato DC3000 secretes coronatine (COR), which is a mimic of the JA-Ile and perceived through the COI1–JAZ co-receptor complex. This COR–COI1–JAZ complex then directs JAZ proteins, such as JAZ2, JAZ5, and JAZ10, for degradation [69,86]. (b) P. syringae also releases type III effector HopX1, a cysteine protease that has been reported to interact with the ZIM domain of JAZ family members and degrade them [87]. (c) HopBB1 is another effector released by P. syringae and interacts with both TCP14 and JAZ3, the repressor components of JA signaling, and glues them together to facilitate their degradation in a COI1-dependent manner [85] (i). HopZ1a interacts with the C-terminal Jas domain of JAZ proteins and directs their degradation in a COI1-dependent manner [8] (ii). Together with RIN4, the AvrB effector activates the plasma membrane ATPase AHA1. This complex then causes an alteration in membrane potential and, through an unknown mechanism, increases the interaction between COI1 and JAZ, ultimately leading to degradation of the JAZ proteins [88] (iii). In all these cases, the degradation of JAZ proteins relieves the repression of transcription factors (TFs) and activation of JA signaling, as described in Figure 2, and leads to enhanced pathogen virulence. AHA1, Arabidopsis plasma membrane H+-ATPase; COI1, CORONATINE INSENSITIVE 1 receptor; COR, coronatine; JAZ, JASMONATE ZINC-FINGER EXPRESSED IN INFLORESCENCE MERISTEM (ZIM)-DOMAIN PROTEIN; InsP₅, Inositol pentakisphosphate; NINJA, NOVEL INTERACTOR OF JAZ; RIN4, RESISTANCE TO P. syringae pv. maculicola 1 (RPM1)-INTERACTING 4; TCP14, TEOSINTE BRANCHED, CYCLOIDEA AND PROLIFERATING CELL FACTORS 14; TPL, TOPLESS; TPR, TPL-RELATED protein.