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Keywords:

  • Arabidopsis;
  • cancer;
  • cross-talk;
  • defence;
  • jasmonate (JA);
  • salicylic acid (SA);
  • senescence;
  • stress

Abstract

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

Contents

 Summary1
I.Introduction2
II.Key players in the jasmonate biosynthetic and signalling pathways2
III.High-throughput studies add new elements to stress-activated signalling networks6
IV.Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways8
V.Jasmonates and senescence10
VI.New physiological scenarios for jasmonates11
VII.Conclusions and perspectives13
 Acknowledgements13
 References13

Summary

Plant development and stress responses are regulated by complex signalling networks that mediate specific and dynamic plant responses upon activation by various types of exogenous and endogenous signal. In this review, we focus on the latest published work on jasmonate (JA) signalling components and new regulatory nodes in the transcriptional network that regulates a number of diverse plant responses to developmental and environmental cues. Not surprisingly, the majority of the key revelations in the field have been made in Arabidopsis thaliana. However, for comparative reasons, we integrate information on Arabidopsis with recent reports for other plant species (when available). Recent findings on the regulation of plant responses to pathogens by JAs, as well as new evidence implicating JAs in the regulation of senescence, suggest a common mechanism of JA action in these responses via distinct groups of transcription factors. Moreover, a significant increase in the amount of evidence has allowed placing of specific mitogen-activated protein kinases (MAPKs) as crucial regulatory nodes in the defence signalling network. In addition, we report on new physiological scenarios for JA signalling, such as organogenesis of nitrogen-fixing nodules and anticancer therapy.


I. Introduction

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

Plant developmental plasticity is an essential feature derived from their intrinsic condition as sessile organisms. To cope with constantly changing environmental conditions, as well as developmental phase transitions, complex signalling networks are activated by different types of exogenous and endogenous signal, leading to extensive transcriptional, proteomic and metabolic changes that ultimately determine a specific plant response to the initial signalling input(s).

Stress and development are regulated in a concerted manner by multiple hormones, and genetic screens performed to identify mutants with defects in a particular hormone or signalling molecule have uncovered, in many instances, interactions between different signalling pathways (Finkelstein et al., 2002; Fu & Harberd, 2003; Guo & Ecker, 2004; Sun & Gubler, 2004; Woodward & Bartel, 2005; Achard et al., 2006; Nakamura et al., 2006; Rolland et al., 2006; Truman et al., 2007). In this review we focus on the key elements mediating cross-talk between jasmonates (JAs) and other signalling pathways in different physiological scenarios. Signalling pathways involved in the stress perception and transduction include those regulated by JAs, salicylic acid (SA), ethylene (ET) and abscisic acid (ABA). These molecules are involved in the local and/or systemic defence responses of the plant (for relevant recent reviews see Devoto & Turner, 2005; Lorenzo & Solano, 2005; Beckers & Spoel, 2006; Fujita et al., 2006; Gfeller et al., 2006; Grant & Lamb, 2006).

Plant hormones regulate development not via linear pathways, but through complex interconnections between different signalling pathways. The concept of signalling networks has evolved from that of pathways. A signalling pathway can be defined as a cascade of events connecting input elements (environmental and developmental stimuli) to output elements (the responses). Until recently, such a cascade was viewed as a simple chain of consecutive steps. However, recent research has focused on the divergence observed at various steps in a pathway, and on the cross-talk, feed-back, pleiotropy and redundancy between signalling pathways (Schwartz & Baron, 1999; Klipp & Liebermeister, 2006). Cross-talk refers to the case where two or more inputs work through a network of interconnected pathways sharing signalling components to regulate specific plant responses and ultimately development. Intensive experimental work has revealed numerous potential paths for cross-talk. Yet, despite the integration of inputs from different hormones in regulating development, it has recently been shown that the transcriptional response in young Arabidopsis seedlings exposed to a regime of seven different hormones (ABA; gibberellic acid-3, GA; indole acetic acid, IAA; 1-amino-cyclopropane-1-carboxylic acid, ACC (precursor of ethylene); zeatin, a cytokinin; brassinosteroids, BL; methyljasmonate, MeJA) over a 3-h period shared a low number of common target genes. This suggests, at least early in hormone perception, a specific and independent response to each hormone. It should be noted, however, that despite the low numbers of shared transcriptional targets, ample evidence was observed of one hormone regulating genes involved in the metabolism of another hormone (Nemhauser et al., 2006). It is possible that the results of this analysis might be limited to the narrow temporal window considered. Clearly, more exhaustive analyses of the molecular components and regulatory nodes of the hormonal signalling networks under study, as well as of the precise cellular and physiological experimental conditions, are necessary before drawing broad conclusions regarding cross-talk between signalling molecules.

JAs are part of the hormonal network that regulates plant developmental plasticity. Their involvement in stress signalling has been studied extensively, supporting their role as key regulators of plant defence responses against pathogens and environmental stresses such as wounding, water deficit and ozone exposure, not only in Arabidopsis but also in other plant species such as tomato (Solanum lycopersicon) and tobacco (Nicotiana attenuata and Nicotiana tabacum). Extensive cross-talk occurs between JAs and SA, another signalling molecule with an important function in plant defence responses. There is evidence for both antagonistic and synergistic interactions between these two signals, suggesting that positive and negative interactions might contribute towards the specificity of the final defence response (for review see Beckers & Spoel, 2006; Wasternack, 2006). Although JAs are also involved in the regulation of fruit ripening, root growth, tuberization, senescence, pollen development and tendril coiling, they have been considerably less studied in these contexts. As with other plant hormones, the identification and characterization of several mutants impaired in JA biosynthesis, perception or signal transduction, as well as analysis of transgenic plants with altered expression of JA-regulated genes, have been instrumental in identifying important components of the JA signalling pathway (for recent reviews see Devoto & Turner, 2005; Lorenzo & Solano, 2005; Schilmiller & Howe, 2005; Delker et al., 2006; Wasternack et al., 2006; Wasternack, 2006; Dreher & Callis, 2007; Wasternack, 2007; for a schematic view of the jasmonate signalling pathway see Gfeller et al., 2006; Liechti et al., 2006).

II. Key players in the jasmonate biosynthetic and signalling pathways

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

1. Jasmonate biosynthetic pathway

Jasmonates are oxylipins (oxygenated fatty acids) that originate from linolenic acid released from chloroplast membranes by lipase enzymes and subsequently oxygenated by lipoxygenases (LOXs) to hydroperoxide derivatives (Fig. 1; for a detailed discussion of the different branches of the LOX pathway refer to Wasternack, 2006, 2007). The initial step in the biosynthesis of JAs via the octadecanoid pathway (Fig. 1a) is catalysed by an allene oxide synthase (AOS) that converts 13-hydroperoxy-linolenic acid (13-HPOT) to an unstable allene oxide intermediate, which is in turn modified by an allene oxide cyclase (AOC) to form 12-oxo-phytodienoic acid (OPDA) (Vick & Zimmerman, 1984). All the reactions leading to the formation of OPDA occur in the plastids, whereas the subsequent steps take place in the peroxisome. Reduction of OPDA by OPDA reductase 3 (OPR3) is followed by three rounds of β-oxidation to finally yield jasmonic acid ((+)-7-iso-JA in Fig. 1; Cruz Castillo et al., 2004; Li et al., 2005; Theodoulou et al., 2005). For detailed reviews on JA biosynthesis refer to Delker et al. (2006); Schaller et al., 2005; Wasternack (2006), (2007).

image

Figure 1. (a) Schematic diagram of the jasmonate (JA) biosynthetic pathway. Biosynthesis of JA from α-linolenic acid requires the enzymes 13-lipoxygenase (13-LOX), allene oxide synthase (AOS) and allene oxide cyclase (AOC) in the chloroplast, and the enzymatic activity of 12-oxo-phytodienoic acid reductase3 (OPR3), acyl-CoA oxidase (ACX), multifunctional protein (MFP) and 3-ketoacyl-CoA thiolase (KAT) in the peroxisome. Intermediates (square boxes): 13-HPOT, 13-hydroperoxylinolenic acid; OPC-8:0, 3-oxo-2- (2′-pentenyl)cyclopentane-1-octanoic acid; OPDA, 12-oxo-phytodienoic acid; JA, (+)-7-iso-jasmonic acid. (b) Metabolism of jasmonates. JA may be metabolized to different compounds depending on the chemical modification of the carboxylic acid group, the pentenyl side chain or the pentanone ring. JA metabolites: MeJA, methyl jasmonate; JA-ACC, conjugate with 1-aminocyclopropane-1-carboxylic acid; JA–Ile, conjugate with the amino acid isoleucine; 12-HSO4-JA, sulfonated derivative of the 12-hydroxy-jasmonic acid; 12-O-GlcJA, glucosylated derivative of the 12-hydroxy-jasmonic acid; JA-O-Glc, glucosylated derivative of JA (adapted from Wasternack, 2007).

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Mutants have been isolated for virtually every step of the jasmonate biosynthetic pathway. Several characterized Arabidopsis JA biosynthetic mutants are male sterile (McConn & Browse, 1996; Sanders et al., 2000; Stintzi & Browse, 2000; Ishiguro et al., 2001; Park et al., 2002; von Malek et al., 2002). For example, the Arabidopsis dad1 (defective in anther dehiscence 1) mutant displays defects in anther dehiscence, pollen maturation, filament elongation and flower opening. This male-sterile phenotype can be rescued by the exogenous application of JA or linolenic acid. The DAD1 gene encodes a chloroplastic phospholipase A1 (Ishiguro et al., 2001). Application of JA also rescues the severe male sterility present in the mutants dde1 (delayed dehiscence 1) and opr3 (oxo-phytodienoic acid reductase 3). Cloning of these mutant loci indicated that they encode the JA biosynthetic enzyme OPR3 (Sanders et al., 2000; Stintzi & Browse, 2000).

Recent analysis of acyl-coenzyme A oxidase (ACX) mutants in Arabidopsis has shown that the JA synthesis mediated by ACX1/5, one of the three key enzymes involved in β-oxidation, is essential for male reproductive development and defence against chewing insects such as Trichoplusia ni (Schilmiller et al., 2007). Additionally, analysis of the mutants aim1 (abnormal inflorescence meristem 1) and pex6 (peroxin 6), which are defective in fatty acid β-oxidation and peroxisome biogenesis, respectively, as well as feeding experiments, have provided further proof of the importance of the peroxisomal β-oxidation step in the octadecanoid biosynthetic pathway (Delker et al., 2006). Previous to the action of the enzymes ACX1/5, MFP (multifunctional protein) and KAT (L-3-ketoacyl CoA thiolase), which are responsible for carrying out the fatty acid β-oxidation in the peroxisome, an activation step of OPDA or its products 3-oxo-2(2′-[Z]-pentenyl) cyclopentane-1-octanoic acid (OPC-8:0) and 3-oxo-2(2′-[Z]-pentenyl)cyclopentane-1-hexanoic acid (OPC-6 : 0) may occur. This mechanism has been suggested by the identification of three 4-coumarate : CoA ligase- (4CL)-like proteins in Arabidopsis, which displayed in vitro specific activation of OPDA and its derivatives as well as peroxisomal localization (Schneider et al., 2005; Koo et al., 2006).

Jasmonic acid can be metabolized to several derivatives (Fig. 1b), with MeJA (a volatile active methyl ester, derivative of jasmonic acid) being one of the best characterized. Among the JA amino acid conjugates, a role in pathogen resistance has been reported for JA–Ile (jasmonoyl–isoleucine). A recent study on N. attenuata transgenic plants impaired in the production of JA–Ile by silenced threonine deaminase indicates that this conjugated derivative of JA is mediating plant defence mechanisms against insects such as Manduca sexta. Also, silencing of JASMONATE RESISTANT 4 (JAR4), the N. attenuata homologue of the Arabidopsis JA-amino synthetase JAR1 (JASMONATE RESISTANT 1) gene, confirmed the role of JA–Ile in activating defence responses (Kang et al., 2006). JAR1 is required in Arabidopsis to activate JA signalling (Staswick & Tiryaki, 2004) and to confer resistance against the soil fungus Pythium irregulare (Staswick et al., 1998). The identification of JAR1 uncovered an enzyme that conjugates JA to isoleucine and clearly revealed that in addition to the well known methylated forms (Falkenstein et al., 1991; Feys et al., 1994; for a recent review see Wasternack, 2007), amino acid conjugates of JA are also bioactive. Similarly, the JA precursor OPDA is able to induce plant defence mechanisms in the absence of jasmonic acid (Stintzi et al., 2001). The involvement of OPDA during wound-induced gene expression has been explored in a recent DNA microarray study, where it has been shown that OPDA triggers the expression of a subset of genes distinct from those induced by JA. These OPDA-specific response genes responded to OPDA but not to JAs (Taki et al., 2005).

2. Jasmonate signalling pathway

Several mutants involved in JA signal perception and transduction have been isolated, the best characterized of which is coi1 (coronatine insensitive 1; for review see Turner et al., 2002; Devoto & Turner, 2005; Lorenzo & Solano, 2005). Mutations of COI1 display resistance to JA inhibition of root growth, various degrees of male sterility, accumulation of anthocyanins, altered senescence and increased susceptibility to several necrotrophic pathogens, biotrophic fungi and pests (Penninckx et al., 1996; Thomma et al., 1998; Norman-Setterblad et al., 2000; Ellis & Turner, 2002; Ellis et al., 2002; Reymond et al., 2004; Zarate et al., 2007). It has been shown that COI1 is required for all the JA-mediated responses analysed so far. Interestingly, characterization of the tomato homologue of COI1 indicates that JAs might have different regulatory functions during reproductive development in different species. In tomato, in addition to jasmonate-related defence responses (a characteristic shared with the Arabidopsis coi1 mutant), COI1 is required for the maternal control of seed maturation and glandular trichome development (Li et al., 2004b). Microarray studies have searched for wound-, jasmonate- and COI1-regulated genes revealing that genes induced by both wounding and MeJA generally required COI1 in Arabidopsis (Devoto et al., 2005). In particular, this study also highlighted the complexity of the signal transduction network mediated by JAs, wounding and COI1. The expression of several JA-induced genes does not appear to require COI1, whereas the induction of several others by wounding does not appear to require jasmonate. In addition, the involvement of OPDA-induced genes during the wound response in Arabidopsis is accomplished via a COI1-independent pathway (Taki et al., 2005). COI1 encodes an F-box protein that is part of an E3 ubiquitin ligase complex involved in ubiquitin-mediated protein degradation. In Arabidopsis the COI1 protein associates with CUL1 (Cullin1), RBX1 (RING-box protein 1) and the Skp1-like proteins ASK1 (Arabidopsis S-PHASE KINASE-ASSOCIATED PROTEIN 1) and ASK2 to form the SCFCOI1 (SKP1, CDC53p/CUL1, F-box) ubiquitin–ligase protein degradation complex (Devoto et al., 2002; Xu et al., 2002). Importantly, JA-related phenotypes have been identified in plants with mutations in components of the ubiquitin proteasome system (Tiryaki & Staswick, 2002; Xu et al., 2002; Lorenzo & Solano, 2005; Moon et al., 2007) linking JAs signalling with ubiquitin-mediated protein degradation.

The Arabidopsis COI1 is closely related to the auxin signalling TIR1 (TRANSPORT INHIBITOR RESPONSE 1) gene (Ruegger et al., 1998), which encodes the first plant F-box protein to be identified as part of an SCF complex (Gray et al., 1999). More recently, TIR1 was demonstrated to act as an auxin receptor (Dharmasiri et al., 2005; Kepinski & Leyser, 2005). AXR1 is a positive regulator of auxin response that modulates SCFTIR1. activity (Leyser et al., 1993) and is additionally considered to be a connection node regulating the activity of different SCF complexes. As a result of the similarities in the mode of action of COI1 and TIR1, it is tempting to speculate that jasmonate and auxin might use analogous signalling mechanisms sharing common components such as AXR1. Interestingly, the auxin-resistant mutant axr1-24 (AUXIN RESISTANT 1) has been isolated in a screen for decreased sensitivity to JA. This allele of axr1 also displays reduced inhibition of root growth by ACC. AXR1 was also found to be necessary for resistance to P. irregulare in Arabidopsis (Tiryaki & Staswick, 2002). This work provided initial evidence for the involvement of auxin signalling components in defence. For a recent review on the role of the ubiquitin/proteasome system in regulating hormonal signalling pathways and responses to biotic stresses, see Dreher & Callis (2007).

Plants use an extremely complex network of synergistic defensive tactics to guard themselves from different pathogens. Fundamental to inducible basal resistance is the ability to recognize and respond to small molecular motifs named pathogen-associated molecular patterns (PAMPs; Nürnberger et al., 2004), recently renamed microbial associated molecular patterns (MAMPs; Mackey & McFall, 2006). Significantly, a recent study has shown that bacterial PAMPS such as bacterial flagellin (flg22) downregulate auxin signalling in Arabidopsis by targeting auxin receptor transcripts (Navarro et al., 2006). Specific suppression of auxin receptors such as TIR1 was shown to occur via post-transcriptional gene silencing mediated by the microRNA miR393. Repression of auxin signalling results in reduced Pseudomonas syringae growth, associating auxin with disease susceptibility via miRNA-mediated suppression of auxin signalling (Navarro et al., 2006). Whether JAs utilize small RNA-mediated sequence-specific mRNA degradation to regulate expression of SCFCOI1 targets remains to be demonstrated.

Potential targets for COI1-mediated ubiquitination have been identified via yeast two-hybrid screen and immuno-assays (Devoto et al., 2002), as well as gene silencing (Xu et al., 2002). Among these putative targets of the SCFCOI1 E3 ligase complex, the histone deacetylase RPD3b/HDAC6 constitutes a particularly interesting substrate, considering its known function as transcriptional repressor (Devoto et al., 2002). Incidentally, constitutive overexpression of histone deacetylase 19 (RPD3A/HDAC19), the closest homologue of the COI1-interacting partner RPD3b in Arabidopsis, decreased histone acetylation levels and enhanced expression of jasmonic acid-responsive PR (pathogenesis-related) genes (Zhou et al., 2005). It has not been shown whether or not RPD3A can also interact with COI1.

Since TIR1 was identified as an auxin receptor (Dharmasiri et al., 2005; Kepinski & Leyser, 2005), the sequence similarity between COI1 and TIR1 has led to hypothesize that the SCFCOI1 might be the jasmonate receptor (Chini et al., 2007; Thines et al., 2007). Recently, members of the jasmonate ZIM-domain (JAZ) protein family have been identified by Thines et al. (2007) as direct targets of SCFCOI1 ubiquitin ligase and the 26S proteasome. The JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Importantly, the JAs (see above), but not other biologically active JA derivatives such as OPDA or MeJA, promotes physical interaction between COI1 and JAZ1 in yeast. At the same time, an independent study identified an Arabidopsis JAZ gene (JAI3/JAZ3) as a repressor of JA signalling (Chini et al., 2007). Collectively, these results suggest that the COI1–JAZ complex might be a site of perception for JA–Ile. Moreover, it was demonstrated that JAI3 interacts with MYC2, and that JAI3 is a negative regulator of MYC2 function. Therefore SCFCOI1-dependent proteasome degradation of JAZ proteins releases MYC2, leading to transcriptional activation of jasmonate responses (Chini et al., 2007). Whether COI1 acts as a receptor only for JA–Ile, and the degree to which other JAZs and JAZ-like proteins contribute to jasmonate signalling, remain to be elucidated. In addition, it is possible that other JAs mediate the interaction between COI1 and other members of the JAZ family, or with SCFCOI1 substrates that await identification.

JASMONATE ASSOCIATED 1 (JAS1), a novel mediator of wounding and JA-regulated growth inhibition, was selected in a MeJA-based growth inhibition screen for transgenic plants expressing candidate JA signalling genes obtained from microarray experiments (Yan et al., 2007). The demonstration that JAS1.1 and JAS1.3 are targeted to the nucleus, and that the expression of JAS1.3 affects transcript levels for at least three other genes, suggests that this protein might act as a transcriptional regulator. Intriguingly, JAS1 corresponds to JAZ10, one of the members of the ZIM domain-containing JAZ protein family. It remains to be demonstrated whether JAS1/JAZ10 also acts as a repressor of JA signalling via COI1, as has been shown for JAZ1 and JAZ3 (Chini et al., 2007; Thines et al., 2007).

So far, only one coi1 suppressor, cos1, has been identified in Arabidopsis. The gene encodes a lumazine synthase, which catalyses the penultimate step in the riboflavin (vitamin B2) biosynthetic pathway. The mutation reverts the coi1 phenotype in terms of JA-induced root growth, gene expression, senescence and defence responses (Xiao et al., 2004).

Constitutive JA-signalling mutants such as cet (constitutive expressor of THI2.1; Hilpert et al., 2001) and cev1 (constitutive expressor of VSP1; Ellis et al., 2002) have been isolated in Arabidopsis. Nine of the 10 cet mutants identified in a genetic screen for constitutive expression of the THI2.1 (THIONIN 2.1) JA-regulated gene display spontaneous leaf cell necrosis, and some display upregulation of the PR1 (pathogenesis-related 1) gene, a common feature of the systemic acquired resistance (SAR) response (Hilpert et al., 2001). SAR is an inducible plant-defence response involving a cascade of transcriptional events mediated by SA. This defence mechanism, often induced after a local infection, provides increased resistance in organs distant from the site of primary infection against subsequent pathogen infections (Durrant & Dong, 2004). Analysis of multiple mutant lines between cet and the fad3-2, fad7-2, fad8 triple mutant (a JA-biosynthetic mutant), coi1 (a JA-signalling mutant) and NahG (transgenic plant expressing salicylate hydroxylase and thus a SA-deficient plant) suggest that at least some of the CET genes act in the cell death stress response in a JA- and SA-dependent manner (Nibbe et al., 2002). The molecular components responsible for the phenotype of the cet mutants remain to be identified.

The mutant cev1 displays constitutive activation of JA signalling, showing increased defence responses against fungal and bacterial pathogens as well as aphids (Ellis et al., 2002). Recently, it has been shown that cev1 is also more resistant to infestation by silverleaf whitefly (an obligate phloem-feeding pest with a different feeding habit from that of aphids; Zarate et al., 2007). This mutant overproduces not only JA, but also OPDA and ethylene, along with constitutive expression of the biotic stress-responsive genes VSP (VEGETATIVE STORAGE PROTEIN), PDF1.2 (PLANT DEFENSIN), Thi2.1 (THIONIN) and CHI-B (CHITINASE B) (Ellis & Turner, 2001; Ellis et al., 2002). It has been found that CEV1 encodes the cellulose synthase CeSA3, providing a link between cell wall signalling and JA and ethylene-regulated defence responses (Ellis et al., 2002).

In Arabidopsis, Lorenzo et al. (2004) have identified five jai1/jin1 (jasmonate insensitive 1) mutant alleles, and have cloned MYC2, a nuclear localized basic helix–loop–helix-leucine zipper (bHLHzip)-type transcription factor that antagonistically regulates two branches of the JA-signalling pathway in a COI1-dependent manner. Although MYC2 was originally isolated as an ABA-response mutant (Abe et al., 2003), it is a positive regulator of a subset of JA-inducible genes and is essential for JA-dependent developmental processes in Arabidopsis. However, the molecular mechanisms underlying the control of MYC2 expression remain largely unknown. Other alleles of jai have been identified and found to encode COI1 (JAI5), JAR1(JIN4/JAI2) and SGT1b (SUPPRESSOR OF THE G2 ALLELE OF skp1-4; JAI4), a yeast regulator of the activity of SCF complexes (Kitagawa et al., 1999). For further information on allelic relationships, refer to reviews by Devoto & Turner (2005); Lorenzo & Solano (2005).

Signalling JA mutants share some common phenotypes, such as reduced root growth inhibition by JA or MeJA, anthocyanin accumulation, enhanced sensitivity to pathogens, and altered expression of JA-responsive genes. Analyses of JA mutants have mostly focused on altered JA-inducible gene expression and defence responses, whereas a detailed analysis of the causes underlying the stunted growth that characterizes some of them has seldom been performed.

III. High-throughput studies add new elements to stress-activated signalling networks

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

The broad availability of mutants, pathosystems and transcription profiling by microarrays in Arabidopsis has made possible faster identification of new molecular components of stress-activated signalling pathways and crucial regulatory nodes integrating signalling networks. Combinations of these tools have been used to identify regulatory nodes in the transcriptional network underlying SAR, and to provide new elements in our understanding of the cross-talk between JAs and SA. SA is required for the activation of SAR and the transcriptional activation of pathogenesis-related (PR) genes such as PR1, PR2 and PR5, which constitutes one of the key molecular events that characterize SAR (Dong, 2004; Beckers & Spoel, 2006). The cascade of transcriptional events caused by SA is mediated by the transcription cofactor NPR1/NIM1/SAI1 (nonexpressor of PR-genes1/noninducible immunity1/salicylic acid-insensitive; this is an allelic series) (Cao et al., 1997; Shah et al., 1997; Kinkema et al., 2000). NPR1 forms a high-molecular-weight oligomeric complex in the cytosol. Changes in cellular redox potential caused by pathogen-induced SA accumulation lead to the formation of NPR1 monomers that are translocated into the nucleus to activate PR genes, whereas the NPR1 homomeric complex remains in the cytoplasm (Kinkema et al., 2000; Mou et al., 2003). The NPR1 5′ UTR contains several W-boxes, which are binding sites for plant-specific WRKY transcription factors. WRKY transcription factors are characterized by the presence of a DNA-binding domain that contains the conserved WRKYGQK sequence as well as a zinc-finger motif (Eulgem et al., 2000). There are 74 WRKY members in Arabidopsis, and several members of this family regulate plant defence (Fig. 2; Ulker & Somssich, 2004; Eulgem & Somssich, 2007). Mutation of W-boxes in NPR1 abolishes binding of WRKY proteins, leading to loss of SA-induced PR gene expression and disease resistance (Yu et al., 2001). Moreover, NPR1 shares similarity with IkB, a target protein that undergoes ubiquitin-mediated protein degradation in the proteasome during anti-inflammatory responses in animals (Regnier et al., 1997).

image

Figure 2. Working model for a regulatory network integrating WRKY-transcription factors under the control of salicylic acid (SA) and jasmonates (JAs) during defence response and developmental senescence. Upon activation of SA- and/or JA-signalling pathways, these two hormones antagonistically regulate expression of WRKY53, which functions as a positive modulator of senescence. Whereas the effect on WRKY70 by SA (via NPR1-dependent and independent pathways) has been demonstrated in the context of defence, its regulatory role on senescence via COI1 remains to be clarified. It is currently unknown if MeJA-induced expression of WRKY62 occurs via COI1. This model is based primarily on results of Kalde et al. (2003); Li et al. (2004a); Wang et al. (2006); Zheng et al. (2006); Mao et al. (2007), Miao & Zentgraf (2007); Ulker et al. (2007), discussed in the text. Arrows indicate induction; blunt ends indicate repression.

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Genetic studies have provided evidence that JA signalling negatively regulates the expression of SA-responsive genes in Arabidopsis (Petersen et al., 2000; Kloek et al., 2001). In addition, the antagonistic effect of SA on JA signalling requires NPR1 (Spoel et al., 2003). Whereas nuclear localization of NPR1 is critical for the induction of PR genes (Kinkema et al., 2000), integration between SA and JA signalling occurs through NPR1 in the cytosol (Spoel et al., 2003).

In order to identify direct transcriptional targets of NPR1 acting as regulatory nodes during SAR, Wang et al. (2006) performed microarray analysis in a stepwise approach on Arabidopsis plants expressing the NPR1-GR (glucocorticoid receptor) fusion protein (Wang et al., 2005). This analysis showed that NPR1 directly upregulates the expression of five WRKY transcription factors that had never before been placed in the SAR network. Interestingly, some of these WRKY factors (WRKY70 and WRKY53) have also been placed in the cross-talk between JA and SA. Both positive (WRKY18 and 53) and negative (WRKY58) regulators of SAR were found. In addition, fine tuning of SAR appears to take place in the presence of high SA levels: signalling through positively acting WRKY factors was found to prevail over the negative effect of WRKY58 in triggering downstream gene transcription. In addition, the action of WRKY70 and WRKY54 prevented excessive SA accumulation (Wang et al., 2006).

A common element in SA- and JA-mediated signalling pathways is the transcription factor WRKY70. WRKY70 is downstream of NPR1 in the SA-dependent signalling pathway; it activates SA-induced genes and inhibits JA-responsive genes. Therefore WRKY70 has been defined as a node for SA- and JA-mediated signalling events during plant responses to bacterial pathogens. WRKY70 mRNA levels are enhanced in a coi1-1 background, suggesting that JA represses its expression (Li et al., 2004a). It has been demonstrated recently by the laboratory of Palva (Li et al., 2006) that gain or loss of WRKY70 function has opposite effects on JA-mediated resistance to the necrotrophic pathogen Alternaria brassicicola and on SA-mediated resistance to the biotrophic Erysiphe cichoracearum. These results corroborate the role of WRKY70 in fine-tuning the SA- and JA-dependent defence pathways (Fig. 2).

It is known that NPR1 interacts with TGA transcription factors (bZIP transcription factors; Zhang et al., 1999) to activate the expression of antimicrobial PR genes (Zhang et al., 1999; Fan & Dong, 2002). The recent analysis by Ndamukong et al. (2007) added a new element to the SA/JA cross-talk. Using a modified yeast two-hybrid screen aimed at identifying TGA-interacting proteins, a member of the glutaredoxin family (GRX480) was isolated and analysed by bimolecular fluorescence complementation (BiFC) analysis in mesophyll protoplasts. As glutaredoxins catalyse thiol-disulfide reductions, it is plausible that they function to regulate the redox state of NPR1 and consequently TGAs. Moreover, it was shown that GRX480 is a negative regulator of the JA-inducible gene PDF1.2.

Another interesting example of cross-talk has been demonstrated between SA-dependent SAR and rhizobacteria-triggered ISR (induced systemic resistance). ISR is activated by the nonpathogenic bacteria Pseudomonas fluorescens, and confers broad-spectrum resistance to pathogen attack (Pieterse et al., 2001, 2002). Analyses of Arabidopsis mutants defective in ethylene and JA signalling have demonstrated that ISR depends on functional JA and ethylene pathways, and requires NPR1 but not SA (Pieterse et al., 1998). Therefore SAR and ISR signalling pathways are distinct in their requirement for SA and JA/ethylene. Concurrent activation of SAR and ISR results in enhanced resistance to pathogenic P. syringae pv. tomato DC3000 (van Wees et al., 2000). In addition to the considerable evidence available regarding antagonistic cross-talk between the JA- and SA-signalling pathways probably involving elements such as WRKY70, NPR1, MPK4 (MITOGEN-ACTIVATED PROTEIN KINASE 4), EDS1 (ENHANCED DISEASE SUSCEPTIBILITY 1) and PAD4 (PHYTOALEXIN DEFICIENT 4), a recent report discusses the nature of the interaction between JA and SA in terms of amplitude and duration (and spatial separation) of each signal (Mur et al., 2006). The authors analysed the effects of cotreatment with JA and SA on JA- and SA-induced genes and oxidative stress in Arabidopsis and tobacco. Synergistic effects were reported at low concentrations and antagonistic interactions were observed at higher concentrations or after prolonged treatment times. Interestingly, the synergistic effects of SA and JA on gene expression and reactive oxygen species (ROS) production were NPR1- and COI1-dependent (Mur et al., 2006). Expression and function of the transcription factor WRKY62 was also found to be synergistically induced by MeJA and SA (Mao et al., 2007). MeJA inducibility of WRKY62 is mediated by cytosolic NPR1. Analysis of wrky62 mutant and WRKY62-overexpressing plants showed that WRKY62 suppresses JA-responsive gene expression. These results suggest that WRKY62 might function downstream of cytosolic NPR1 and regulate SA-mediated inhibition of JA signalling. Interestingly, WRKY62 expression is induced after inoculation with Hyaloperonospora parasitica, indicating a role for WRKY62 during plant defence (Kalde et al., 2003)

Two key points in the establishment of SAR that remain unclear are the nature of the mobile signal, and the precise identity of the remotely activated signalling networks in undamaged parts of the plant (Grant & Lamb, 2006). In a recent study performed in Arabidopsis, Truman et al. (2007) have shown that systemically responding leaves rapidly activate an SAR transcriptional signature with strong similarity to local basal defence responses (see section II) and to responses triggered by herbivores and wounding. This molecular signature shares secondary metabolism components with late basal defence responses. Interestingly, this activation occurs in the absence of PAMPs contact (Nürnberger et al., 2004). The RPM1 (RESISTANCE TO P. syringae pv. maculicola 1) pathosystem (Grant et al., 1995) has been used to dissect both the timing and the nature of early transcriptional events associated with the establishment of systemic immunity after RPM1 recognition. Using this system, Truman et al. (2007) have ascribed a role for JAs as the initial signal triggering SAR. JAs are thus implicated in working upstream of SA-dependent responses in systemic leaves. These conclusions were achieved through an extensive comparison of in-house microarray analysis with experiments on host responses to biotic and abiotic stresses or hormone treatments available from the ArrayExpress (http://www.ebi.ac.uk/arrayexpress; Parkinson et al., 2007) and NASCArrays (http://affymetrix.arabidopsis.info) databases. Novel work by Grant's laboratory has shown that SAR can be mimicked by JA application and can be abolished in mutants impaired in either JA synthesis or response. In addition, de novo JA biosynthesis was found to be linked to the induction of jasmonate-responsive genes in systemic tissues. Therefore, although JAs have generally been regarded as antagonizing SA-dependent responses, the differential activation of JA- and SA-signalling pathways in terms of early or late induction and local or systemic activation might provide plants with an adaptive defence mechanism. Furthermore, genetic analysis of mutants defective in JA biosynthesis, JA signal perception and systemin (peptide involved in systemic wound signalling), as well as grafting studies conducted in tomato, indicate that jasmonates are also essential components of the systemic wound signal (for review see Schilmiller & Howe, 2005). Plant responses to herbivore attack or mechanical wounding include the production of proteinase inhibitors (PIs) and toxic substances that have negative effects on herbivores, as well as of volatile compounds that attract predators. The systemic nature of the wound response is supported by a signal transduction pathway that relies on the local activation of JA biosynthesis at the lesion site and on the existence of a mobile wound signal that requires JA perception for its recognition in distal nonwounded leaves (Li et al., 2002). Interestingly, a tomato loss-of-function mutant of acyl-CoA oxidase (ACX1A) lacks local and systemic expression of PIs in response to wounding. Grafting experiments with acx1 JA-deficient plants demonstrated that a disrupted β-oxidation step in the JA-biosynthetic pathway interferes with production of the wound transmissible signal, but not with its recognition in the distal leaves. Also, these grafting experiments indicated that JA (or a derivative of JA), and not the precursor OPDA, is the signal for systemic wound response in tomato (Li et al., 2005).

In a recent study aimed to further dissect Arabidopsis defence response to Botrytis cinerea, changes in mRNA profiles of wild-type plants were compared with those of the coi1 and ein2 (ethylene insensitive 2) mutants (which display enhanced susceptibility to necrotrophic pathogens) and to plants carrying the NahG gene (showing impaired disease-resistance response) (AbuQamar et al., 2006). In wild-type plants, the expression of 621 genes representing approx. 0.48% of the Arabidopsis transcriptome was induced in response to Botrytis. The expression of 181 Botrytis-induced genes (BIGs) was dependent on a functional COI1 gene, whereas the expression of 63 and 80 BIGs was dependent on ET signalling and SA accumulation, respectively. Thirty BIGs encode putative DNA-binding proteins such as zinc-finger, MYB, WRKY, and HD-ZIP families of transcription factors previously found to be regulating ET responses. Importantly, T-DNA insertion mutants in two BIGs encoding putative DNA-binding proteins ZFAR1 and WRKY70 showed increased susceptibility to Botrytis infection. ZFAR1 is also required for germination in the presence of ABA, and encodes a putative transcription factor containing zinc-finger and ankyrin-repeat domains. In summary, this work highlights the complex signalling network regulating defence responses to Botrytis in Arabidopsis, which involves the transcriptional activation of genes implicated in hormone synthesis and signalling, removal of ROS, and responses to biotic and abiotic stresses. Intriguingly, also in this study, the transcript levels of the transcription factor WRKY33 were also increased significantly following Botrytis infection. In another study from Mengiste's laboratory, mutations of WRKY33 were found to cause enhanced susceptibility to B. cinerea and A. brassicicola. This was associated with decreased expression of the plant defensin PDF1.2 gene, providing yet more evidence for the role of WRKY transcription factors as regulators in the cross-talk between SA- and JA-modulated defence responses. The repression of WRKY33 by COI1 is similar to the situation reported for WRKY70. However, unlike WRKY70, endogenous SA does not appear to be required for basal and induced expression of WRKY33 (Zheng et al., 2006).

Whereas the SAR and other defence responses have an obvious and critical importance as adaptive mechanisms of plant protection against constant pathogen challenge, few studies have tried to asses the fitness consequences of defence responses. Because of this, it is interesting to mention a recent study performed in Arabidopsis to assess the fitness benefits of SAR (Heidel & Dong, 2006). In this study, the authors compared wild-type plants with mutants with abolished SAR (the npr1/nim1 mutant), constitutively active SAR (the cpr1 and cpr5 mutants, constitutive expressor of PR; Clarke et al., 2000) and the transgenic line NPR1-H (displays enhanced SAR response upon activation), under pathogen challenge and different nutrient levels. Wild-type plants showed higher fitness than npr1 mutant plants under low-nutrient conditions and pathogen attack. Under high-nutrient conditions, there was neither benefit nor a negative effect of SAR on fitness. These results, plus the previous finding in a field experiment that npr1 plants had decreased fitness compared with wild-type plants (Heidel et al., 2004), prompted the authors to suggest that SAR has an adaptive purpose (Heidel & Dong, 2006). Constitutive SAR response did not confer a fitness benefit in the cpr plants under different nutrient conditions, indicating that the high fitness cost of constitutive resistance is independent of nutrient availability. Whereas the high fitness cost of constitutive SAR in the cpr mutants correlates well with SAR-induced PR expression, PDF1.2 expression is not clearly associated with that high fitness cost (Heidel et al., 2004; Heidel & Dong, 2006). As mentioned earlier, JA and ET are also, in addition to SA, key inducers of plant-defence responses (mostly against necrotrophic pathogens, herbivores and wounding) that involve the expression of the PDF1.2 gene. Even though the fitness cost of applications of JA to induce resistance has been evaluated in terms of seed yield (Redman et al., 2001), the fitness effects at the gene expression level remain to be determined.

IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

In plants, MAPK (mitogen-activated protein kinase) and CDPK (calcium-dependent protein kinase) cascades regulate biotic and abiotic stress responses and various developmental processes. The MAPK signalling pathway is a linear cascade of three types of protein kinase: MAPK, MAPK kinase (MAPKK), and MAPKK kinase (MAPKKK) (Chen et al., 2001; Jonak et al., 2002; Nakagami et al., 2005). Work performed mostly in Arabidopsis has contributed to clarifying the role of several kinases in JA signalling and/or in the cross-talk between JA and other signalling pathways. Indeed, pharmacological studies using protein kinases or protein phosphatase inhibitors have revealed the roles of protein phosphorylation and dephosphorylation in JA signalling (Leon et al., 2001). In addition, several reports have shown that MAPKs are involved in JA or wound signalling in various plant species (Seo et al., 1995; Bögre et al., 1997; Seo et al., 1999; Petersen et al., 2000; Holley et al., 2003; Gomi et al., 2005; Kandoth et al., 2007). In particular, the first observations by Seo et al. (1995) demonstrated that a rapid, systemic increase in transcripts encoding WIPK (wound-induced protein kinase), a MAP kinase homologue in tobacco, occurs in response to mechanical wounding. These findings corroborated the hypothesis that the initial wound signal stimulates the phosphorylation of protein kinases and activates enzymes involved in jasmonate biosynthesis (Farmer & Ryan, 1992). However, only recently, a role for JA in the activation of plant MAPKs has been demonstrated in Arabidopsis. The Arabidopsis dwarf, JA-insensitive mutant mpk4 (MAP kinase 4) contains high levels of SA, and shows constitutive expression of PR1 along with increased resistance to P. syringae and the oomycete H. parasitica (Petersen et al., 2000). The constitutive activation of SAR, along with the repression of JA-induced genes in mpk4, led to the consideration that MPK4 acts as a regulator in the cross-talk between SA and JA pathways. A recent study by Brodersen et al. (2006) contributed to further dissecting the MPK4-mediated defence pathway and its function in regulating SA-, JA- and ET-dependent responses. Through double mutant analysis and comparative microarrays, the authors demonstrated that essential components of salicylic acid-mediated defence responses such as EDS1 and PAD4 act as regulators of the antagonism between SA and ET/JA-mediated defence responses, downstream of MPK4. This study also shows that MPK4 activity is required for the repression of SAR and the induction of ET/JA defence pathways. In addition, the MAPKKK MEKK1 is required for flg22-induced activation of MPK4 but not of MPK3 or MPK6. MEKK1 acts upstream of MPK4 as a negative regulator of pathogen-response pathways, a function that may not require MEKK1's kinase activity (Suarez-Rodriguez et al., 2007).

Recently, Takahashi et al. (2007) identified a JA-activated Arabidopsis MAPK cascade, MAPK KINASE3–MAPK6 (MKK3–MPK6). MPK6 has previously been identified as a component of disease resistance in Arabidopsis (Menke et al., 2004). Using microarray analysis, qRT-PCR and genetic analyses of gain-of-function and loss-of-function mutants in the MKK3–MPK6 cascade, Takahashi et al. (2007) showed that JA represses the expression of the transcription factor MYC2. MYC2 was previously found to promote JA-dependent gene expression (see above) and to repress JA/ET-dependent genes (Boter et al., 2004; Lorenzo et al., 2004). Indeed, MPK6 was activated by JA in a COI1-dependent manner, and this activation was also MKK3-dependent (Takahashi et al., 2007). Moreover, the authors have demonstrated that the MKK3–MPK6 cascade plays a role in regulating JA-/ET-dependent gene expression, and present a model to explain how MPK6 mediates signals such as JA, pathogen and cold/salt. In this model, MPK6 operates within three distinct cascades. The MKK2–MPK6 and MKK4/MKK5–MPK6 cascades positively regulate cold and salt stress responses and ethylene-mediated induction of PDF1.2, respectively. The MKK3–MPK6 cascade negatively regulates JA-mediated root growth and gene expression of VSP2 via MYC2. The MYC2 transcription factor fine-tunes the cross-talk with the ethylene pathway by repressing PDF1.2 (Lorenzo et al., 2004).

In Arabidopsis, wounding activates several MAP kinases such as MPK4, MPK6 and MPK1/MPK2 (Bögre et al., 1997; Ichimura et al., 2000; Ortiz-Masia et al., 2007). In particular, JA also activates MPK1/MPK2 in the absence of wounding. Wound- and JA-induction of MPK1/2 has been found to be COI1-independent (Ortiz-Masia et al., 2007). As mentioned above, several genes induced by wounding have also been described to be JA-regulated independently of COI1 (Devoto et al., 2005). Other stress signals, such as ABA and hydrogen peroxide, activated MPK1/2, suggesting a role for MPK1/2 kinase activity in different kinds of stress (Ortiz-Masia et al., 2007).

It is widely accepted that JA and ET are required for plant defence responses to necrotrophic pathogens. Moreover, Arabidopsis and tomato mutants altered in ET and JA signalling or biosynthesis show increased susceptibility to Botrytis and other necrotrophic pathogens (Thomma et al., 1999; Diaz et al., 2002; Ferrari et al., 2003). Using a combination of microarray and reverse genetics analysis, Veronese et al. (2006) have shown that a mutation in the membrane-anchored BOTRYTIS-INDUCED KINASE 1 (BIK1) reduces JA- and ET-regulated defence responses. These conclusions are based mainly on the expression of the plant defensin PDF1.2 gene. bik1 mutants also show alterations in root growth, and in the number and size of root hairs, indicating that BIK1 is also required for root development. Additionally, BIK1 function is independent of COI1, EIN2 and PAD2 (PHYTOALEXIN DEFICIENT 2). SIPK (SA-induced protein kinase) and WIPK, two tobacco MAPKs, and their respective orthologues in other plant species, have been proposed to function as central convergence points in stress signalling (Jonak et al., 2002). It was initially demonstrated by Seo et al. (1995) that inactivation of WIPK in tobacco plants leads to inhibition of the production of wound-induced JA and inhibition of the accumulation of wound-inducible gene transcripts. By contrast, the levels of SA and transcripts for PR proteins were increased on wounding. Moreover, Seo et al. (2007) have shown recently that, in tobacco, the wound-activated MAPKs WIPK and SIPK contribute to regulation of the levels of JA and SA in response to wounding. Interestingly, silencing of WIPK or SIPK by RNA interference impairs wound-induced accumulation of jasmonic acid (Seo et al., 2007). Also, in N. tabacum, the calcium-dependent protein kinase NtCDPK2 activates both ethylene and JA pathways, and acts as a link between abiotic and biotic signal responses. Additionally, NtCDPK2 mediates via ethylene the inhibition of SIPK and WIPK activation (Ludwig et al., 2005). Recently, Kandoth et al. (2007) used virus-induced gene silencing to show that tomato MPK1 and MPK2 function in the systemin-signalling pathway, probably upstream of JA biosynthesis. MPK1 and MPK2 are required for expression of a subset of wound-response genes and resistance to M. sexta. Therefore the interplay between signalling pathways, including MAPK- and CDPK-dependent cascades, might control the induction of distinct stress responses.

The mitogen-activated protein kinase phosphatases (MKPs) are negative regulators of MAPKs (Camps et al., 2000). In dicotyledonous plants such as Arabidopsis and tobacco, MKPs have been shown to play roles in hormonal and abiotic stress responses, and in microtubule organization (Ulm et al., 2001; Monroe-Augustus et al., 2003; Naoi & Hashimoto, 2004). However, information about the role of MKPs in monocotyledons is just emerging. In rice, the expression of OsMKP1 is induced by wounding. OsMKP1 binds calmodulin (CaM) in a manner similar to its tobacco homologue NtMKP1, possibly acting as a negative regulator of wound responses. This role for OsMKP1 is supported by the observation that in the mkp1 loss-of-function mutant, wound-responsive genes are upregulated. As a putative CaM-binding domain is also present in AtMKP1 as well as in homologues of other plant species, CaM binding appears to be a unique and conserved feature of plant MKPs (Katou et al., 2007). However, in contrast with the Arabidopsis mkp1 loss-of-function mutant, which shows altered response to genotoxic stresses (Ulm et al., 2001), the rice mkp1 mutant showed a semidwarf phenotype (Katou et al., 2007). Significantly, a recent study by Schweighofer et al. (2007) described the Arabidopsis MAPK Ser/Thr phosphatase AP2C1 as a novel stress signal regulator inactivating MPK4 and MPK6. ap2c1 mutant plants showed enhanced wound-induced JA levels and higher resistance to phytophagous mites (Tetranychus urticae). Overexpression of AP2C1 impaired resistance to Botrytis and caused reduced production of ethylene.

In summary, the work reported above shows that there is now a significant amount of evidence placing specific MAPKs as crucial regulatory nodes in JA-mediated stress responses, even though the distinctive regulatory elements between different plant species remain to be identified.

V. Jasmonates and senescence

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

The involvement of JAs in regulating developmental processes has not been explored to the same depth as their roles in plant defences. Leaf senescence is, in essence, a type of programmed cell death that progresses at a much slower rate than, for example, the hypersensitive response (HR) induced by pathogens (Hopkins et al., 2007). However, there is significant overlap between pathogen-related and senescence-related genes (Weaver et al., 1998; Quirino et al., 1999), indicating that there might be some common elements in the signalling pathways that regulate senescence-associated and HR-associated programmed cell deaths. Leaf senescence is a developmental program that is regulated by intrinsic factors such as hormones and developmental age, and environmental factors such as temperature, light, nutrients and pathogens. Although the effects of several phytohormones on leaf senescence have been known for a long time, the molecular mechanisms underlying the hormonal regulation of leaf senescence are not yet completely understood (Lim et al., 2007). In recent years, gene-expression analysis during leaf senescence has provided further evidence for the involvement of JA (as well as for the cross-talk between JA, SA and ET) in the regulation of this complex and highly regulated developmental program.

The fact that not all the cells within a senescing leaf show the same degree of senescence at any given point has prompted the use of different methods, such as dark-induced senescence or sucrose starvation-induced senescence in cell suspension cultures, to induce senescence in a synchronous manner. Gene-expression profiles in senescent cell-suspension cultures (induced by sucrose starvation) are more similar to those for dark-induced senescence than to those for developmental leaf senescence. However, while some genes that depend on JA and ET for expression are found to be expressed in developmental, dark-induced and starvation-induced senescence (hydrolases and enzymes involved in carbohydrate metabolism), the SA-signalling pathway appears to have an active role only during developmental senescence (Buchanan-Wollaston et al., 2005). These results clearly indicate a complex regulation of the senescence process, with similarities as well as significant differences in gene expression depending on the type of senescence under consideration.

In Arabidopsis, increased JA levels, differential activation of biosynthetic JA enzymes, and induction of SENESCENCE ASSOCIATED GENES (SAGs) characterize senescing leaves (He et al., 2001, 2002). Moreover, JA induction of precocious leaf senescence following exogenous JA treatment fails to generate senescence symptoms in the JA-insensitive coi1 mutant, indicating that JA induces senescence in a COI1-dependent manner (He et al., 2002). The complexity of the regulation of this pathway was highlighted in a recent study, where it was found that senescence-regulated genes were also repressed by wounding and MeJA. The repression of senescence associated gene SEN1 (SENESCENCE 1) was COI1-independent. Other similarly regulated genes included SAG29 and a cysteine proteinase gene similar to SAG12 (Devoto et al., 2005).

In addition to its association with components of the SCFCOI1 ubiquitin ligase complex and with a histone deacetylase (see section II, 2), COI1 also interacts with the small subunit of rubisco (Devoto et al., 2002). The finding that the small subunit of rubisco might be a potential target of COI1-dependent proteolysis is interesting, because it might provide the link explaining the reduced levels of rubisco found after the exogenous application of jasmonic acid or MeJA (reviewed by Parthier, 1990). In this respect, it has also been reported that a gene encoding for the chlorophyll a/b-binding protein (CAB) is continuously downregulated during developmental and dark-induced senescence (van der Graaff et al., 2006).

The ore9 mutant, which displays increased longevity during age-dependent senescence and ABA-, MeJA- and ethylene-induced senescence, carries a mutation in a gene encoding an F-box domain and leucine-rich repeat-containing protein. The interaction of ORE9 with the ASK1 component of the SCF complex suggests that ubiquitin-dependent proteolysis is probably involved in controlling leaf senescence (Woo et al., 2001). A transcriptome analysis during developmental leaf senescence in Arabidopsis yielded increased transcript abundance of 30 genes involved in ubiquitination control, emphasizing the specific targeting of proteins for degradation by the 26S proteosome as an important mechanism in the control of senescence (Buchanan-Wollaston et al., 2005).

Another recent Arabidopsis transcriptome analysis comparing developmental and induced leaf senescence (van der Graaff et al., 2006) adds more detail to the hormonal pathways that regulate senescence, and reveals the senescence-type specificity of some of the genes in the JA pathway. Whereas developmental leaf senescence, darkening-induced senescence of individual leaves attached to the plant, and senescence in dark-incubated detached leaves share many common senescence-regulated genes such as SAGs, this study highlighted the differential activation of the JA biosynthetic enzymes depending on the senescence scenario. Different JA biosynthetic enzymes were activated during developmental leaf senescence and wounding, but not during darkening-induced senescence of individual leaves attached to the plant. Interestingly, the only JA-signalling gene that is strictly downregulated in all the senescence conditions tested was COS (van der Graaff et al., 2006). This expression profile supports the proposed role of COS1 as a suppressor of some JA responses, including senescence (Xiao et al., 2004; van der Graaff et al., 2006).

Transcriptome analyses have revealed that > 800 genes increase their transcript abundance during developmental leaf senescence in Arabidopsis (Buchanan-Wollaston et al., 2005). Among these genes, the WRKY family of transcription factors constitutes one of the largest groups that exhibit upregulation during senescence (Guo et al., 2004; Lin & Wu, 2004; (Buchanan-Wollaston et al., 2005). In particular, the WRKY53 transcription factor has been analysed further in terms of its involvement in controlling leaf senescence (Hinderhofer & Zentgraf, 2001; Robatzek & Somssich, 2002; Miao et al., 2004) and the identification of its interacting partners during senescence (Miao & Zentgraf, 2007). Yeast two-hybrid and co-immunoprecipitation analyses have shown that WRKY53 interacts with ESR/ESP (EPITHIOSPECIFYING SENESCENCE REGULATOR), a JA-inducible protein that is involved in plant responses to pathogens, and in senescence. These two proteins have an antagonistic function during leaf senescence, and their roles are modulated by the JA/SA equilibrium. Moreover, the ESR effect on leaf senescence occurs via WRKY53 (Miao & Zentgraf, 2007), an SA-inducible WRKY factor, expression of which is upregulated at a very early stage of leaf senescence (Hinderhofer & Zentgraf, 2001). Because WRKY53 expression is regulated antagonistically by JA and SA, and the WRKY53 protein interacts with the JA-inducible ESR protein in the nucleus, it has been proposed that WRKY53 might be a node for JA- and SA-mediated signals in senescence (Miao & Zentgraf, 2007), a situation clearly similar to that discussed in section IV for WRKY70 in plant defence. New evidence indicates that WRKY70 also acts as a negative regulator of developmental senescence (Ulker et al., 2007; Fig. 2).

VI. New physiological scenarios for jasmonates

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

1. Nodule organogenesis

The symbiotic relationship between nitrogen-fixing rhizobial bacteria and the roots of leguminous plants results in the development of specific plant root structures (called nodules), where the bacterial enzyme nitrogenase fixes atmospheric nitrogen, providing the plant with a source of nitrogen. Initiation of nodulation is dependent on the release of lipochito-oligosaccharide Nod factors by the rhizobial bacteria, in response to plant-derived production of flavonoids into the rhizosphere (Stougaard, 2000). Recent reports have demonstrated activation of the cytokinin signalling pathway to be a requirement for the initiation of nodule development (Murray et al., 2007; Tirichine et al., 2007). Auxins, abscisic acid, brassinosteroids, ethylene and gibberellins are also involved in nodule development (Oldroyd et al., 2001; Suzuki et al., 2004; Ferguson et al., 2005; van Noorden et al., 2006). In particular, ET appears to regulate nodulation in a negative fashion via inhibition of Nod factor-induced calcium spiking (Oldroyd et al., 2001; Oldroyd & Downie, 2006). However, elucidation of the complex hormonal network that regulates nodule organogenesis and senescence is still incomplete.

Recently, it has been shown that JA inhibits nodulation in Medicago truncatula (Sun et al., 2006) and that shoot-applied MeJA suppresses root nodulation in Lotus japonicus (Nakagawa & Kawaguchi, 2006). It has been reported that JA and ET work additively to inhibit nodulation, but antagonistically in the regulation of Nod factor induced-calcium-spiking frequency and responsiveness to a Nod factor signal in the root hair cells of the host (Sun et al., 2006). An analysis of a cDNA array of 18144 ESTs from L. japonicus shows that a number of genes involved in pathogen defence responses (including phytoalexin biosynthesis enzymes, enzymes involved in cell wall modification, PR proteins) and the expression of genes encoding AOC and OPRs (JA biosynthetic enzymes) were upregulated during the early steps of the RhizobiumLotus interaction. However, the high levels of induction during the infection process are suppressed during the nodule formation step. Genes encoding lipoxygenase, which catalyses the initial step of jasmonate biosynthesis, were the most significantly downregulated genes (Kouchi et al., 2004). This analysis of gene-expression profiles during the early stages of nodulation corroborates the repressive effect of JAs on nodulation, and also indicates a common trend in the transient induction of defence genes and nodule-specific genes during the infection and primordial initiation steps of nodulation.

Interestingly, JA might also have a role in the establishment of arbuscular mycorrhizal (AM) symbiosis. AM is a fungus of the phylum Glomeromycota and exists in a symbiotic association with vascular plants (Schüssler et al., 2001), where the plant provides the fungus with carbohydrates and the fungus improves the mineral nutrition of the plant. Increases in the endogenous levels of JA have been correlated with the establishment of AM in M. truncatula (Stumpe et al., 2005) and barley (Hause et al., 2002). Interestingly, in a recent report where expression of one of the two genes encoding for the JA biosynthetic enzyme AOS in M. truncatula was partially suppressed, a decrease in the rate of colonization and arbuscule formation was observed (Isayenkov et al., 2005).

2. Anti-cancer therapy

It is well known that methyl jasmonate is a chemical inducer of secondary metabolism in plant species such as Catharanthus roseus (Vázquez-Flota & De Luca, 1998; Collu et al., 2001; Goossens et al., 2003; Hernández-Dominguez et al., 2004; Rischer et al., 2006). The medicinal plant C. roseus contains a number of terpenoid indole alkaloids (TIAs), some of which exhibit strong pharmacological activity (van der Heijden et al., 2004). In particular, vinblastine and vincristine, antineoplastic bisindole alkaloids, are already in clinical use. In C. roseus, TIA accumulation is strongly influenced by the interaction of phytohormones such as auxins and jasmonates (Gantet & Memelink, 2002).

The molecular structure of jasmonates is reminiscent of the animal defence-mediating prostaglandins. However, the biological mechanisms involved in regulating JA- and prostaglandin-dependent responses appear to be different (Funk, 2001; Mueller, 2004; Loeffler et al., 2005; Sattler et al., 2006). Jasmonates are also structurally related to isoprostanes/phytoprostanes, products of nonenzymatic lipid peroxidation pathways that are initiated by ROS (Thoma et al., 2003; Mueller, 2004). These compounds have been shown to display a variety of biological activities in mammalian cells, and have also been reported to play a role in oxidative stress signalling, not only in animals but also in plants (Thoma et al., 2003). Similarly, reactive electrophile species (compounds containing α,β-unsaturated carbonyl groups or other reactive electrophilic atom groups derived from enzymatic or nonenzymatic fatty acid oxygenation) have been implicated as signals in biotic and abiotic stresses (Farmer & Davoine, 2007).

In plants, a role for JAs in regulating cell-cycle progression is just emerging. JA blocks G1/S and G2/M transitions, and cell sensitivity toward JA is dependent on cell-cycle phase (Świątek et al., 2002). In addition, JA prevents accumulation of B-type cyclin-dependent kinases and of cyclin B1;1 (Świątek et al., 2004), but the molecular mechanism by which this is accomplished is not known. Interestingly, JA, which plays a role in organ senescence and wound response, also induces cell death and suppresses cell proliferation in several human cancer cell lines, supporting the potential use of JA and its synthetic derivatives as anticancer drugs (for other recent reviews see Flescher, 2007; Wasternack, 2007). The first report on the anticancer activity of jasmonates showed that this group of plant hormones suppressed proliferation and induced apoptosis in human cancer cells (Fingrut & Flescher, 2002). Since then, several studies have been performed to try and determine the mode of action of jasmonates against cancer cells (Ishii et al., 2004; Rotem et al., 2005) as well as the cooperative effect of JAs in different combinations with currently available chemotherapeutic drugs (Heyfets & Flescher, 2007; Reischer et al., 2007). It has been proposed that jasmonates provoke death in cancer cells, not by changes in cellular mRNA transcription, protein translation or p53 expression, but by acting directly and selectively on mitochondria in cancer cells (Rotem et al., 2005). Specifically, it has been reported that jasmonates are toxic to mitochondria in human cancer cell lines because they induce mitochondrial membrane depolarization via abnormal opening of the permeability transition pore complex channel and therefore provoke cytochrome c release from mitochondria to the cytosol and ATP depletion, leading ultimately to cancer cell death (Rotem et al., 2005). MeJA-induced apoptosis in cancer cells via production of ROS has also been implicated as one of the mechanisms by which JAs induces cancer cell death. It has been shown that MeJA induces apoptosis in A549 human lung adenocarcinoma cells through induction of the expression of pro-apoptotic members of the Bcl-2, Bax and Bcl-XS protein families and the activation of caspase-3 via ROS production (Kim et al., 2004). Furthermore, it has been demonstrated that MeJA induces heat-shock protein 72 (HSP72) in C6 glioma cells through heat-shock factor 1 (HSF10) in a ROS-dependent manner (Oh et al., 2005).

Another model of action proposed for jasmonates as anticancer agents is the induction of a redifferentiated state (characterized by a slower proliferation rate and loss of neoplastic characteristics) in myeloid leukemia cells by MeJA via MAPK activation (Ishii et al., 2004). It was recently reported that cis-jasmonate and methyl jasmonate induction of apoptosis and cell-cycle arrest in cell lung cancer lines is associated with phosphorylation of p38 and ERK1/2 (extracellular signal-regulated kinase1/2), increased expression of Bax and p21, and activation of caspase-3 (Yeruva et al., 2006). Thus the mechanisms described above to explain the anticancer properties of JAs might overlap in some specific cellular scenarios.

Finally, it is interesting to note that JA effects on basic cellular machineries such as induction of cell-cycle arrest (Fingrut & Flescher, 2002; Naill & Roberts, 2005; Yeruva et al., 2006), activation of MAPK cascades (Ishii et al., 2004), and production of ROS species (Kim et al., 2004; Oh et al., 2005) in animal cancer cells are shared with plants, where similar effects have also been reported (Fig. 3; Asai et al., 2000; Świątek et al., 2002, 2004; Song & Goodman, 2002; Danon et al., 2005). However, details on the extent of these similarities, and on the specificity of the molecular mechanisms active at one time in different cell types in response to distinct stimuli, are not yet completely understood. Indeed, further investigation of the molecular mechanisms regulating the action of JAs in plant cells could lead to the development of novel anticancer drugs.

image

Figure 3. Effects of jasmonates (JAs) on plant and cancer cells. JAs induce defence/cell death and alteration of cell-cycle dynamics in plant and animal cells. This process could be mediated by reactive oxygen species (ROS) and/or activation of mitogen-activated protein kinases (MAPKs). In cancer cells, JAs could cause cell death either by altering mitochondrial function or ROS production, or by inducing redifferentiation through MAPK signalling. Thicker lines indicate mechanisms identified in both cell types; thinner lines indicate possible diversification in the mechanisms controlling the final outputs in either animal or plant cells. Arrows indicate induction; blunt ends indicate repression. Refer to section VI, 2 for further details. This model elaborates on the results of Asai et al. (2000); Fingrut & Flescher (2002); Song & Goodman (2002); Świątek et al. (2002, 2004); Ishii et al. (2004); Kim et al. (2004); Danon et al. (2005); Naill & Roberts (2005); Rotem et al. (2005); Yeruva et al. (2006); Flescher (2007).

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VII. Conclusions and perspectives

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References

Studies on the effects of JAs on various stress responses and developmental processes have shown that in most JA-mediated processes, regulation of a specific plant response is the result of a complex and dynamic interaction between different signalling pathways. Recent research in JA and SA signalling has uncovered new elements and crucial nodes for the regulation of signalling networks in different physiological scenarios. One such emerging signalling network integrating different plant responses appears to be regulation by WRKY transcription factors, at least in the context of defence and senescence. However, important gaps in our understanding of JA signalling remain to be filled, such as the identity of a universal JA receptor(s) and the integration of different MAPKs, CDPKs, ROS species and TGA and WRKY transcription factors into the various signalling networks we have described. Finally, the anticancer activity of JAs, as well as JA involvement in nodule organogenesis, provide exciting new physiological scenarios for exploration.

References

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Key players in the jasmonate biosynthetic and signalling pathways
  5. III. High-throughput studies add new elements to stress-activated signalling networks
  6. IV. Novel contribution of kinase cascades to cross-talk between jasmonate and other defence-signalling pathways
  7. V. Jasmonates and senescence
  8. VI. New physiological scenarios for jasmonates
  9. VII. Conclusions and perspectives
  10. Acknowledgements
  11. References
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