Báo cáo khoa học: Plant oxylipins: Plant responses to 12-oxo-phytodienoic acid are governed by its specific structural and functional properties ppt

MINIREVIEW Plant oxylipins: Plant responses to 12-oxo-phytodienoic acid are governed by its specific structural and functional properties Christine Bottcher1 and Stephan Pollmann2 ă CSIRO Plant Industry, Adelaide, Australia Department of Plant Physiology, Ruhr-University Bochum, Germany Keywords 12-oxo-phytodienoic acid; cyclo-oxylipingalactolipids; environmental stress; jasmonates; jasmonic acid; mechanotransduction; oxylipins; phytoprostanes; plant stress responses; transcriptional regulation Correspondence S Pollmann, Department of Plant Physiology, Ruhr-University Bochum, Universitaetsstrasse 150, D-44801 Bochum, Germany Fax: +49 234 321 4187 Tel: +49 234 322 4294 E-mail: stephan.pollmann@ ruhr-uni-bochum.de (Received November 2008, revised 23 March 2009, accepted 31 March 2009) One of the most challenging questions in modern plant science is how plants regulate their morphological and developmental adaptation in response to changes in their biotic and abiotic environment A comprehensive elucidation of the underlying mechanisms will help shed light on the extremely efficient strategies of plants in terms of survival and propagation In recent years, a number of environmental stress conditions have been described as being mediated by signaling molecules of the oxylipin family In this context, jasmonic acid, its biosynthetic precursor, 12-oxo-phytodienoic acid (OPDA), and also reactive electrophilic species such as phytoprostanes play pivotal roles Although our understanding of jasmonic acid-dependent processes and jasmonic acid signal-transduction cascades has made considerable progress in recent years, knowledge of the regulation and mode of action of OPDA-dependent plant responses is just emerging This minireview focuses on recent work concerned with the elucidation of OPDA-specific processes in plants In this context, aspects such as the differential recruitment of OPDA, either by de novo biosynthesis or by release from cyclo-oxylipin-galactolipids, and the conjugation of free OPDA are discussed doi:10.1111/j.1742-4658.2009.07195.x Introduction Plants are permanently exposed to a multitude of variable environment cues, and thus have to cope with changes in, for example, temperature, light quality, exposure to UV light, mechanical forces and water availability, as well as osmotic stress, wounding and pathogen challenges [1–8] Over time, plants have evolved several physical barriers as defensive weapons, i.e the cuticula, thorns and stinging hairs, as well as constitutively expressed toxic compounds or enzymes In addition to these morphological adaptations, plants have established inducible systems Despite the fact that plants possess neither an immune system nor a nervous system like animals, they are able to defeat herbivore and pathogen predators and respond to changes in their environment using highly complex inducible defense ⁄ response mechanisms These systems require the perception of external stress conditions, transformation of these Abbreviations cGL, cyclo-oxylipin-galactolipid; dnOPD, dinor-OPDA; GSH, glutathione; GST, glutathione S-transferase; JA, jasmonic acid; LOX, lipoxygenase; Me-JA, methylester of JA; OPDA, 12-oxo-phytodienoic acid; RES, reactive electrophilic species; TGA, TGACG motif-binding factor FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4693 OPDA triggered responses in plants C Bottcher and S Pollmann ă stimuli into internal signals, and as a consequence, an appropriate adjustment of gene expression via specific signal-transduction cascades in answer to the altered environment With regard to inducible response mechanisms of plants and animals, compounds derived from the metabolism of polyunsaturated fatty acids, collectively termed oxylipins or octadecanoids, play a crucial role In mammals, oxylipins derive mainly from arachidonic acid, a fourfold unsaturated C20 fatty acid, and have pivotal functions in the inflammatory process, in general reactions to infections and in allergic responses [9] By contrast, phytooxylipins derive mainly from oxygenized C16 and C18 fatty acid precursors Much recent research has focused on the analysis of these compounds The biosynthesis of most plant oxylipins is initiated by the action of lipoxygenases (LOX), which are capable of introducing molecular oxygen at either the C9 or C13 position of the C18 fatty acids linoleic acid (18:2) and a-linolenic acid (18:3), respectively [10,11] Plants possess a number of different LOX isoforms that can be subdivided into two groups: type 1, containing all 9-LOX isoenzymes, which are exclusively found outside the plastids; and type 2, including all plastid-localized isoenzymes, such as the 13-LOXs [12,13] Numerous biochemical studies provide evidence that the hydroperoxy reaction products of LOX-assisted catalysis lead to a plethora of different oxylipins, i.e hydroxy, epoxy or divinylether fatty acids, as well as volatile aldehydes and alcohols and the well-established wound hormones jasmonic acid (JA), 12-oxo-phytodienoic acid (OPDA), dinor-OPDA (dnOPDA), traumatic acid and traumatin [4,14] Moreover, a-dioxygenases catalyze the enantioselective 2-hydroperoxidation of long-chain fatty acids, giving rise to additional oxylipins also involved in pathogen defense [15,16] In recent years, the main concern has been with the 13-LOX reaction, which initiates the synthesis of octadecanoids (Fig 1), a compound class comprising jasmonates such as JA and several JA derivatives like tuberonic acid, a 12-hydroxy analog of JA, and their precursors, for example, the biological active OPDA The biosynthesis of JA, and activation of the intermediates by generation of the corresponding CoA esters for b-oxidation, is deemed to be basically uncovered with respect to the enzymes involved (for a review see Ref [7]) In 1980, the senescence-promoting activity of the methyl ester of JA (Me-JA) was first described for leaves and shoots of Artemisia [17], followed by publications on the growth-inhibiting physiological role of JA in higher plants [18,19] Since then, lots of evidence 4694 has been provided for the involvement of this phytohormone in either mechanotransduction [20], the response to osmotic stress [21], UV damage [22] and water stress [23], or as a defense to wounding [24,25] In particular, with regard to insect attacks [26,27] and infections with necrotrophic fungi [28–30], respectively, JA has been shown to play a key role Furthermore, essential developmental processes, such as seed maturation [31,32], pollen development [33] and anther dehiscence [34] are linked to variations in endogenous JA levels Multiple gemone-wide transcript-profiling approaches, utilizing differential experimental set-ups and several corresponding Arabidopsis mutants have underscored the essential role of OPDA and JA [35] Particularly, the fad3 ⁄ 2fad7 ⁄ 2fad8 (fatty acid desaturase) triple mutant that is unable to produce the JA precursor a-linolenic acid [33] and the coi1 (coronatine insensitive) JA signal transduction mutant [36] have revealed considerably decreased resistance towards the herbivore Bradysia impatiens and the necrotrophic fungus Alternaria brassicicola Based on these results and the JA deficiency of two null alleles in the OPR3 locus, namely opr3 [37] and dde1 (delayed dehiscence) [38], it seemed surprising that these mutants exhibited no altered resistance towards herbivore and pathogen challenge Recently, it has been reported that octadecanoid-dependent growth inhibition is seemingly mediated by JA rather than OPDA Consecutive treatment of opr3 with OPDA resulted in unaffected leaf areas, whereas in OPDA- or Me-JA-treated wild-type plants, leaf areas were significantly reduced By contrast, opr3 mutants infested with B impatiens larvae were able to survive the attack, whereas in the aos mutant the population was reduced to 4% [39] This moved OPDA center stage, and it appears to be a good candidate for an independent signaling molecule specifically mediating resistance towards biotic foes Physiological processes mediated by OPDA Several physiological processes are known to be likewise stimulated by overlapping activities of OPDA and JA In addition, OPDA has been described in JA-independent responses Emphasizing its involvement in mediating resistance to pathogens and pests, OPDA is assumed to be the primary signal transducer in the elicitation process [40], because OPDA strongly induces alkaloid biosynthesis in Eschscholtzia californica cell cultures Furthermore, tendril coiling of Bryonia dioica is more responsive to OPDA than JA Although exogenously administered JA is capable of promoting FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS C Bottcher and S Pollmann ă OPDA triggered responses in plants Fig JA biosynthesis and OPDA metabolism in A thaliana 13-LOX, 13-lipoxygenase; ACX, acyl-CoA oxidase; AOC, allene oxid cyclase; AOS, allene oxid synthase; CTS ⁄ PXA1 ⁄ PED3, ABC transporter for OPDA or OPDA–CoA import; COI1, F-box protein in JA signal transduction; GST, glutathione S-transferase; KAT, L-3-ketoacyl-CoA thiolase; MFP, multifunctional protein; OPR, 12-oxo-phytodienoate reductase; PLAI, plastidic acyl hydrolase tendril coiling, the concentration needed to elicit the reaction is one order of magnitude higher than with methyl-OPDA and exhibits a slower kinetic In addition, JA levels remain lower in mechanoreacting tendrils than in those of cis-(+)-OPDA and increase only late during the coiling process Comparable results have been obtained in Phaseolus vulgaris thigmomorphogenesis In these studies, JA levels remained below the detection limit after mechanical stimulation Thus, OPDA can be considered as an endogenous signal transducer of Br dioica and P vulgaris mechanotransduction (Fig 2) [20,41–43] In this regard, OPDA and JA signaling is perhaps linked with Ca2+ signaling It has recently been reported that OPDA, as well as JA, induces transient Ca2+ signals in both the cytosol and the nucleus of a stimulated transgenic tobacco cell culture By contrast, JA–Ile treatment had no detectable effect on the cellular Ca2+ content of the examined cell culture system [44] Although OPDA and JA both contribute to an FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4695 OPDA triggered responses in plants C Bottcher and S Pollmann ă Fig Schematic representation of stress-induced processes mediated by reactive electrophilic species, such as phytoprostanes and OPDA, and jasmonic acid as well as by its bioactive amino acid conjugate, jasmonoyl–isoleucine increase in the free cellular calcium level, it has been shown that the response to OPDA was much quicker (< 30 s) and the response amplitude higher (1 lm) than in the response to JA treatment This may be indicative of distinct regulatory functions for the two compounds In terms of tendril coiling, the octadecanoid-dependent alteration in the Ca2+ content may 4696 induce ion fluxes, thereby directly affecting the turgor pressure, or regulate the transcription of a specific subset of genes (Fig 2) [45,46] Intriguingly, Medicago truncatula has recently been reported to respond very sensitively to mechanostimulation with enhanced JA levels and altered accumulation of AOC transcripts [47] Unfortunately, this study did not monitor other genes involved in JA biosynthesis or cis-(+)-OPDA levels during the reaction It will be exciting to learn whether mechanotransduction in Medicago is mediated by JA rather than by OPDA Even though nyctinastic leaf movement most likely differs mechanistically from mechanostimulated tendril coiling, work conducted on the nyctinasty of several plant species, such as Albizzia, has emphasized that JA derivatives, i.e potassium b-d-glucopyranosyl 12-hydroxyjasmonate, may at least contribute to this distinct type of plant movement In particular, nyctinastic leaf closing is mediated by potassium b-d-glucopyranosyl 12-hydroxyjasmonate In the case of nyctinasty, it is suggested that the biochemical factors accounting for leaf closing and opening directly affect K+ channel activity, thereby modulating turgor pressure in specialized flexor cells [48–50] By analyzing a rice mutant with an impaired light response, hebiba, it has recently been shown that oxylipins are also involved in phototropic coleoptile bending Further experiments have emphasized an auxin-antagonistic impact of JA in gravitopic reactions It is suggested that the JA gradient that is formed in reciprocal orientation to the indole-3-acetic acid gradient in coleoptiles inhibits growth in places where it is already poorly promoted by indole-3-acetic acid Thereby, the velocity of the gravitopic movement is seemingly accelerated [51–54] The majority of the effects described by the Nick group are most likely not OPDA specific, but rather mediated by JA However, intriguingly, the authors described an OPDA gradient which accompanies the JA gradient in the opposite direction during gravitopism This has been interpreted as a putative second level of regulation in a late step establishing the JA gradient Extending this previous interpretation, it is tempting to speculate that this may also be indicative of OPDA-specific, JA-independent regulatory effects In the conducted experiments, an independent signaling function of OPDA was not taken into account and thus cannot be ruled out Extending the previous functions, OPDA and ⁄ or 16:3 fatty acid-derived dnOPDA are discussed as inhibitors of programmed cell death in the conditional Arabidopsis flu mutant [55] Upon a dark-to-light shift, flu mutants generate singlet oxygen (1O2) in their plastids This non-radical reactive oxygen species accounts FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS C Bottcher and S Pollmann ă for growth inhibitory effects and the development of necrotic lesions [56] Studies on flu and the flu ⁄ dde2-2 double mutant indicated that OPDA and ⁄ or dnOPDA promote the inhibition of programmed cell death processes induced by 1O2, and the well-known cell death induction by JA was suppressed Unexpectedly, comparison of flu and the flu ⁄ dde2-2 double knockout, impaired in OPDA, dnOPDA and JA production, showed that the concurrent absence of those compounds restored the wild-type sensitivity of flu to cell death Hence, OPDA and ⁄ or dnOPDA are seemingly necessary and able to antagonize JA-promoted effects on cell death (Fig 2) (for more detail, refer to the minireview by Reinbothe et al [56a]) A proposed mechanism of OPDA action Despite being processed by the SCFCOI1–JAZ–MYC complex (for more detail, refer to the minireview by Chini et al [56b]), the major regulatory effect of OPDA on the transcriptional machinery is determined by its remarkable structural properties Oxylipins with a,b-unsaturated keto or epoxy functions can behave like reactive electrophilic species (RES) towards cellular nucleophiles [57] In this regard, a,b-unsaturated keto groups can participate in nucleophilic Michael additions in which carbanions are added to a,b-unsaturated carbonyl compounds This type of addition reaction to proteins or to the tripeptide glutathione (GSH) may cause changes in protein activity or in the cellular redox state, which, in turn, can influence gene expression [58–60] Such interactions have been described for OPDA and a variety of related compounds [61–63] Although the enzymatic production and physiological impact of the octadecanoid-phytohormones OPDA and JA is well-known (Fig 1), the nonenzymatic generation of structurally related compounds and their role in cellular stress responses is a very intriguing and challenging matter of actual research The latter compounds comprise oxidized lipids and lipid fragments, many of which are derived in vivo from a-linolenic acid [64] They range from very small compounds such as malondialdehyde [65,66], to more complex families of hydroxy fatty acids and phytoprostanes [67–69] Currently, it is assumed that omega fatty acids, in particular a-linolenic acid, serve in the protection of cells by absorbing reactive oxygen species such that they are oxidized in a free-radical-dependent manner [70] This trienoic fatty acid-mediated consumption of reactive oxygen species results in the nonenzymatic generation of oxidized polyunsaturated fatty acids and the subsequent production of many RES [71] Recent work on the impact of cyclopentenone-oxylipins, i.e OPDA OPDA triggered responses in plants and A1-phytoprostane (Fig 2), on the proteome of Arabidopsis leaves provides evidence for the induction of both classical stress proteins and enzymes connected to cellular redox and detoxification systems by those compounds Notably, a large portion of the identified candidate proteins are located in plastids Given the fact that the two utilized oxylipins are generated in these organelles, one may suggest that direct alteration of enzyme activity ⁄ specificity or direct influencing of the degradation of target proteins, triggered by enzymatically or nonenzymatically generated RES, may take place in chloroplasts [72] In mammals, the structural requirement for activity of cyclopentenone prostaglandins, including effects on gene expression, is already known to be determined by their a,b-unsaturated carbonyl groups [73] Hydroperoxy arachidonic acids, like leukotriene C4 and 5-oxo-7glutathionyl-8,11,14-eicosatrienoic acid, are further examples of such biologically active RES, which can modulate the chemotaxis of neutrophiles and actin polymerization, respectively [74] Moreover, in animals, covalent binding of RES is an appropriate tool with which to regulate transcription factor activity, as shown for nuclear factor kappa-light-chain-enhancer of activated B cells (NF-jB), c-Jun or peroxisome proliferator-activated receptor (PPARc) [75–77] However, experimental evidence for a covalent linkage between RES and any specific protein in planta is yet to be provided Nevertheless, both the examples from animals and work on phytoprostanes allow for hypotheses in which bioactive plant RES act as Michael acceptors, thereby adding not only to GSH, but also directly to enzymes and transcription factors OPDA: an independent regulator of gene expression Given the functional and structural differences between OPDA and JA, it is exciting to presume that OPDA is specifically able to orchestrate the expression of a subset of genes, independent of those influenced by JA To identify such genes, and thus speculate on the physiological impact of their gene products, several microarray approaches, using mainly the opr3 null mutant, have been conducted By analyzing a set of 150 defense-related genes, two general conclusions were drawn First, the COI1 signal transduction pathway can be activated by both OPDA and JA Second, complete activation of the wound response needs the joint action of OPDA and JA Furthermore, not all COI1dependent genes were induced in wounded or OPDAtreated opr3 plants, but both treatments activated the transcription of several COI1-independent genes, which FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4697 OPDA triggered responses in plants C Bottcher and S Pollmann ă were not inuenced by JA [78] More recently, a genome-wide microarray experiment identified a set of > 150 genes that were induced by exogenously applied OPDA, but not by JA or Me-JA [79] The majority of the identified genes encode for proteins involved in stress responses, for example, heat shock proteins, glutathione S-transferases (GSTs) or polypeptides related to signal transduction, such as transcription factors and kinases In addition, genes encoding for enzymes involved in the modulation of cellular indole3-acetic acid levels, such as ILR1, IAR3 and ILL5, suggest a tight connection between stress responses and auxin metabolism Intriguingly, a further study aimed at analyzing the molecular bases of phytoprostane activity, underlines that the regulation of gene expression by those compounds is seemingly similar to the regulation by OPDA and pathogens [63] Moreover, a major part of these responses is shown to be dependent on TGACG motif-binding factor (TGA) transcription factors Thus, a specific interaction of RES, such as OPDA or nonenzymatically formed phytoprostanes, with TGA transcription factors seems plausible and is reminiscent of the mentioned situation in animals (vide ante) However, unless direct covalent binding between RES and any transcription factor has been proven experimentally, the function of RES may also be more indirect; acting through regulation of the cellular redox state Work conducted in the Pieterse lab underscores the tight connection between plant defense responses and the redox state of the cell [80,81] For example, the salicylic acid-induced antagonistic effect on JA-responsive gene expression is facilitated by the modulation of cellular GSH levels The transcriptional regulator, NPR1, undergoes conformational changes in response to alterations in the cellular redox state [82] Under systemic acquired resistance conditions, NPR1 oligomers are reduced to monomers, thereby allowing efficient uptake into the nucleus where NPR1 can develop its gene-regulatory functions Because of the lack of DNA-binding domains in NPR1, it is suggested that the protein acts through protein–protein interaction with transcription factors Indeed, in multiple yeast two-hybrid screens, an interaction between NPR1 and a TGA subclass of basic leucine-zipper transcription factors has been emphasized [83,84] Taking into account that oxylipins effectively induce TGA transcription factor expression, it is attractive to speculate that, as yet undetected, NPR1-like transcriptional regulators are also involved in the redox-dependent transmission of oxylipin signals Very recently, PHO1;H10, a member of the PHO1 gene family of Arabidopsis thaliana, has been described 4698 as being transcriptionally regulated by OPDA, but not by JA or coronatine, a bacterial polyketide metabolite that mimics JA–Ile [85] PHO1;H10 expression is strongly induced by a variety of stresses, including responses to wounding and dehydration The corresponding gene product is involved in loading inorganic phosphate into the xylem in roots Excitingly, PHO1;H10 induction by wounding, as well as OPDA treatment, made use of the COI1-dependent pathway, which is noteworthy in that there is currently no experimental evidence that OPDA can act via the SCFCOI1– JAZ–MYC-complex [86] (see minireview by Chini et al [56b]) However, these results suggest that distinct signaling cascades may emerge from the SCFCOI1 complex, depending on the presence of either OPDA or JA Regulating the pool of free OPDA by conjugation Cell injury, for example, by pathogen attack is, in most cases, accompanied by oxylipin bursts These drastic increases in cellular oxylipin content, governed by enzymatic or nonenzymatic de novo production or by the release of oxylipins from storage compounds (vide infra) go hand in hand with the considerable cell toxicity of these compounds Rapid trapping and sequestration of the partially toxic compounds could prevent unintended cell damage In this connection, animals have evolved mechanisms for the rapid detoxification of oxylipins, e.g by the addition of intracellular thioredoxin [87] With respect to recently presented data, it seems as though the conjugation and thereby inactivation of free signaling molecules is a common feature not only of animals, but also of plants OPDA and phytoprostanes are functionally inactivated by the GST-catalyzed addition of GSH [63,72] In underlying studies, numerous GST genes were found to be upregulated by OPDA One, a predicted chloroplastic GST (GST6, At2g47730), is described as being able to catalyze the conjugation of OPDA to GSH This finding, however, corresponds to work conducted in our laboratory, in that we identified and characterized three OPDA-induced cytoplasmic GSTs of the tau family [88], all capable of adding OPDA, as well as traumatin, to GSH in vitro (C Bottcher et al., unpublished ă data) Based on publicly available microarray data, the expression of all of these GSTs responds strongly to numerous stresses, e.g wounding, jasmonate treatment, nutrient starvation and fungal infections Corresponding OPDA–GSH conjugates have been reported to accumulate in cryptogein-treated tobacco plants [62], the fate of such membrane-impermeable GSH FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS C Bottcher and S Pollmann ă OPDA triggered responses in plants Fig Structures of the currently identified cyclo-oxylipin-galactolipids from Arabidopsis thaliana adducts in plants remains unclear Nevertheless, it may be suggested that the addition of RES to GSH renders them inactive or modulates their biological impact In addition to GST induction, the transcription of lipid transfer proteins is strongly induced in answer to various biotic and abiotic stresses Such lipid transfer FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4699 OPDA triggered responses in plants C Bottcher and S Pollmann ă proteins have already been reported as a potential oxylipin scavenger [89], although addition of OPDA or bioactive phytoprostanes has yet to be explored In conclusion, the results point to a scenario in which RES trigger both the regulation of a specific cluster of genes and their own inactivation by a feedback loop, inducing the expression of detoxification enzymes such as GSTs and lipid transfer proteins OPDA can be released from cyclo-oxylipin-galactolipids Cyclic oxylipins not occur exclusively in their free form Rather, the major portion of these compounds, at least in Arabidopsis and some near relatives, is found covalently bound to galactolipids in the thylakoid membrane [90–95] (Fig 3) The occurrence of lipid-bound cyclic oxylipins is currently assumed to be a special trait of only a very few members of the Brassicaceae Recently, we were able to detect lipidbound cyclic oxylipins in Arabidopsis arenosa, Arabidopsis halleri, Arabidopsis petraea, Arabidopsis thaliana, Arabis pendula, Camelina microcarpa, Capsella rubella and Neslia paniculata, all members of the Brassicaceae, but not in 16 species taken from 11 other families [96] The amount of these esterified oxylipins, collectively termed cyclo-oxylipin-galactolipids (cGL), is not constant but responds to external stimuli Upon wounding, for example, cGL levels in the thylakoids increase [90,97] Furthermore, senescence-promoting effects have been described for arabidopside A (Fig 3), a monogalactosyldiacylglycerol species carrying OPDA at sn1 and dnOPDA at sn2 [98] Furthermore growth inhibitory effects have been reported for monogalactosyldiacylglycerol-O, arabidopside A, B and F (Fig 3) [94] Recent work also linked levels of lipid-bound OPDA and dnOPDA with responses to pathogen challenge, attributing antimicrobial activity to the trioxylipin-containing monogalactosyldiacylglycerol derivatives, arabidopside E and G (Fig 3), which were further shown to accumulate in response to dexamethasone-induced expression of an antivirulence protein [93,95] The biosynthesis of lipid-bound oxylipins is, however, not yet fully understood, but several lines of evidence emphasize a direct conversion of lipid-bound polyunsaturated fatty acids into oxylipins [93] However, the oxylipins linked to the galactosyl-moieties in arabidopside E and G, at least, have to be covalently linked to the molecules by transacylations From this, a general involvement of transacylation reactions, introducing oxylipins into galactolipids, cannot be excluded beyond reasonable doubt Likewise, the participation of enzymes of the jasmonate biosynthetic 4700 pathway in the production of esterified cyclo-oxylipins is yet to be discovered Given that the majority of OPDA and dnOPDA is found trapped in galactolipids, there is speculation about the function of cGL as a storage form for reactive oxylipins and that an alternative free fatty acid-independent pathway exists for the synthesis of oxylipins Consistent with the former hypothesis, the lipolytic release of oxylipins from several cGLs has already been reported [99] Moreover, there is an indication that cGLs may serve as substrates for JA biosynthesis Recently, a plastidic acyl hydrolase has been identified that preferentially catalyzes the hydrolyzation of cGLs (Fig 1) and confers resistance to Botrytis cinerea [100] Intriguingly, the plaI knockout mutant exhibited an expected enhanced susceptibility to the necrotrophic fungus, without affecting wound-induced JA accumulation In fact, this invites the presumption that lipid-bound and free pools of oxylipins are differentially recruited depending on the particular stimulus, which extends the current picture of inducible defense ⁄ response systems in planta Conclusions In Arabidopsis, the majority of cyclic oxylipins are not found the free form, but rather are covalently bound to galactolipids Under certain circumstances, the oxylipins can be released from these lipids by lipases Regardless of their origin, in both plants and animals, RES are engaged in the activation of a distinct set of mostly defense- and stress-related genes Transcriptional regulation is possibly arranged by adding the RES to certain transcription factors, thereby modulating their activity It will be intriguing to discover whether these strikingly similar regulation mechanisms are the result of convergent evolution or whether they constitute an ancient, conserved regulation mechanism that is common to all beings Acknowledgements The authors are grateful to Professor Dr Elmar W Weiler and Dr Florian Schaller for several fruitful discussions Furthermore, the authors thank Professor Dr Eckhard Hofmann for critical comments on the manuscript This work was funded by grants from the Deutsche Forschungsgemeinschaft (DFG), Bonn SFB480 ⁄ A10 and PO1214 ⁄ 3-2 for SP References Browse J (2005) Jasmonate: an oxylipin signal with many roles in plants Vitam Horm 72, 431–456 FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS C Bottcher and S Pollmann ¨ Lorenzo O & Solano R (2005) Molecular players regulating the jasmonate signalling network Curr Opin Plant Biol 8, 532–540 Schaller F, Schaller A & Stintzi A (2005) Biosynthesis and metabolism of jasmonates J Plant Growth Regul 23, 179–199 Schilmiller AL & Howe GA (2005) Systemic signaling in the wound response Curr Opin Plant Biol 8, 369–377 Delker C, Stenzel I, Hause B, Miersch O, Feussner I & Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana – enzymes, products, regulation Plant Biol (Stuttg) 8, 297–306 Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I & Miersch O (2006) The wound response in tomato – role of jasmonic acid J Plant Physiol 163, 297–306 Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development Ann Bot (Lond) 100, 681–697 Balbi V & Devoto A (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios New Phytol 177, 301– 318 Smith T, McCracken J, Shin YK & DeWitt D (2000) Arachidonic acid and nonsteroidal anti-inflammatory drugs induce conformational changes in the human prostaglandin endoperoxide H2 synthase-2 (cyclooxygenase-2) J Biol Chem 275, 40407–40415 10 Feussner I & Wasternack C (2002) The lipoxygenase pathway Annu Rev Plant Biol 53, 275–297 11 Liavonchanka A & Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis J Plant Physiol 163, 348–357 12 Schewe T (1998) Basic functions of lipoxygenases and their products in higher plants In Eicosanoids and Related Compounds in Plants and Animals (Rowley AF, Kuhn H & Schewe T eds), pp 133150 Princeton ă University Press, Princeton, NJ 13 Hildebrand DF, Fukushige H, Afitlhile M & Wang C (1998) Lipoxygenases in plant development and senescence In Eicosanoids and Related Compounds in Plants and Animals (Rowley AF, Kuhn H & Schewe T eds), ă pp 151181 Princeton University Press, Princeton, NJ 14 Vellosillo T, Martinez M, Lopez MA, Vicente J, Cascon T, Dolan L, Hamberg M & Castresana C (2007) Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade Plant Cell 19, 831–846 15 Hamberg M, Sanz A & Castresana C (1999) a-Oxidation of fatty acids in higher plants Identification of a pathogen-inducible oxygenase (piox) as an a-dioxygenase and biosynthesis of 2-hydroperoxylinolenic acid J Biol Chem 274, 24503–24513 OPDA triggered responses in plants 16 Hamberg M, Ponce de Leon I, Rodriguez MJ & Castresana C (2005) a-Dioxygenases Biochem Biophys Res Commun 338, 169–174 17 Ueda J & Kato J (1980) Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.) Plant Physiol 66, 246–249 18 Dathe W, Ronsch H, Preiss A, Schade W, Sembdner ă G & Schreiber K (1981) Endogenous plant hormones of the broad bean, Vicia faba L (-)-jasmonic acid, a plant growth inhibitor in pericarp Planta 153, 530– 535 19 Yamane H, Takagi H, Abe H, Yokota T & Takahashi N (1981) Identification of jasmonic acid in three species of higher plants and its biological activities Plant Cell Physiol 22, 689–697 20 Falkenstein E, Groth B, Mithofer A & Weiler EW ă (1991) Methyljasmonate and a-linolenic acid are potent inducers of tendril coiling Planta 185, 316–322 21 Parthier B (1991) Jasmonates, new regulators of plant growth and development: many facts and few hypotheses on their actions Bot Acta 104, 446–454 22 Conconi A, Smerdon MJ, Howe GA & Ryan CA (1996) The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation Nature 383, 826–829 23 Moons A, Prinsen E, Bauw G & van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots Plant Cell 9, 2243–2259 24 Creelman RA, Tierney ML & Mullet JE (1992) Jasmonic acid ⁄ methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression Proc Natl Acad Sci USA 89, 4938–4941 25 Albrecht T, Kehlen A, Stahl K, Knofel HD, Sembdner ă G & Weiler EW (1993) Quantification of rapid, transient increases in jasmonic acid in wounded plants using a monoclonal antibody Planta 191, 86–94 26 Howe GA, Lightner J, Browse J & Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack Plant Cell 8, 2067–2077 27 McConn M, Creelman RA, Bell E, Mullet JE & Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis Proc Natl Acad Sci USA 94, 5473–5477 ´ 28 Vijayan P, Shockey J, Levesque CA, Cook RJ & Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis Proc Natl Acad Sci USA 95, 7209–7214 29 Staswick PE, Yuen GY & Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare Plant J 15, 747–754 ´ 30 Penninckx IA, Thomma BP, Buchala A, Metraux JP & Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4701 OPDA triggered responses in plants 31 32 33 34 35 36 37 38 39 40 41 42 C Bottcher and S Pollmann ă induction of a plant defensin gene in Arabidopsis Plant Cell 10, 2103–2113 Creelman RA & Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress Proc Natl Acad Sci USA 92, 4114–4119 Hause B, Demus U, Teichmann C, Parthier B & Wasternack C (1996) Developmental and tissue-specific expression of JIP-23, a jasmonate-inducible protein of barley Plant Cell Physiol 37, 641–649 McConn M & Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant Plant Cell 8, 403–416 Ishiguro S, Kawai-Oda A, Ueda J, Nishida I & Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis Plant Cell 13, 2191–2209 ´ Pauwels L, Inze D & Goossens A (2009) Jasmonateinducible gene: what does it mean? Trends Plant Sci 14, 87–91 Feys B, Benedetti CE, Penfold CN & Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen Plant Cell 6, 751–759 Stintzi A & Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis Proc Natl Acad Sci USA 97, 10625–10630 Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW & Goldberg RB (2000) The arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway Plant Cell 12, 1041–1061 Zhang Y & Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis PLoS ONE 3, e3699 Blechert S, Brodschelm W, Holder S, Kammerer L, ¨ Kutchan TM, Mueller MJ, Xia ZQ & Zenk MH (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways Proc Natl Acad Sci USA 92, 4099–4105 Weiler EW, Albrecht T, Groth B, Xia ZQ, Luxem M, Liß H, Andert L & Spengler P (1993) Evidence for the involvement of jasmonates and their octadecanoid precursors in the tendril coiling response of Bryonia dioica Phytochemistry 32, 591–600 Stelmach BA, Muller A, Hennig P, Laudert D, Andert ă L & Weiler EW (1998) Quantitation of the octadecanoid 12-oxo-phytodienoic acid, a signalling compound in plant mechanotransduction Phytochemistry 47, 539– 546 4702 43 Blechert S, Bockelmann C, Fusslein M, Schrader T, ă Stelmach BA, Niesel U & Weiler EW (1999) Structure– activity analyses reveal the existence of two separate groups of active octadecanoids in elicitation of the tendril-coiling response of Bryonia dioica Jacq Planta 207, 470–479 44 Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W & Mithofer A (2007) Structural requireă ments of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells Angew Chem Int Ed Engl 46, 4783–4785 45 Lecourieux D, Ranjeva R & Pugin A (2006) Calcium in plant defence-signalling pathways New Phytol 171, 249–269 46 Mazars C, Bourque S, Mithofer A, Pugin A & Ranjeva R (2009) Calcium homeostasis in plant cell nuclei New Phytol 181, 261–274 47 Tretner C, Huth U & Hause B (2008) Mechanostimulation of Medicago truncatula leads to enhanced levels of jasmonic acid J Exp Bot 59, 2847–2856 48 Ueda M & Nakamura Y (2006) Metabolites involved in plant movement and ‘memory’: nyctinasty of legumes and trap movement in the Venus flytrap Nat Prod Rep 23, 548–557 49 Ueda M & Nakamura Y (2007) Chemical basis of plant leaf movement Plant Cell Physiol 48, 900–907 50 Nakamura Y, Miyatake R & Ueda M (2008) Enantiodifferential approach for the detection of the target membrane protein of the jasmonate glycoside that controls the leaf movement of Albizzia saman Angew Chem Int Ed Engl 47, 7289–7292 51 Riemann M, Muller A, Korte A, Furuya M, Weiler ă EW & Nick P (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba Plant Physiol 133, 1820–1830 52 Gutjahr C, Riemann M, Muller A, Duchting P, Weiler ă ă EW & Nick P (2005) Cholodny-Went revisited: a role for jasmonate in gravitropism of rice coleoptiles Planta 222, 575–585 53 Riemann M, Gutjahr C, Korte A, Riemann M, Danger B, Muramatsu T, Bayer U, Waller F, Furuya M & Nick P (2007) GER1, a GDSL motif-encoding gene from rice is a novel early light- and jasmonate-induced gene Plant Biol (Stuttg) 9, 32–40 54 Riemann M, Bouyer D, Hisada A, Muller A, Yatou O, ă Weiler EW, Takano M, Furuya M & Nick P (2009) Phytochrome A requires jasmonate for photodestruction Planta 229, 1035–1045 55 Danon A, Miersch O, Felix G, op den Camp RG & Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana Plant J 41, 68–80 56 op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, ¨ Feussner I et al (2003) Rapid induction of distinct FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ê 2009 FEBS C Bottcher and S Pollmann ă stress responses after the release of singlet oxygen in Arabidopsis Plant Cell 15, 2320–2332 56a Reinbothe C, Springer A, Samol I & Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence FEBS J 276, doi:10.1111/j.1742-4658.2009.07193.x 56b Chini A, Boter M & Solano R (2009) Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module FEBS J 276, doi:10.1111/j.1742-4658.2009 07194.x ´ 57 Farmer EE, Almeras E & Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory Curr Opin Plant Biol 6, 372–378 58 Hayes JD & McLellan LI (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress Free Radical Res 31, 273–300 59 Itoh K, Tong KI & Yamamoto M (2004) Molecular mechanism activating Nrf2–Keap1 pathway in regulation of adaptive response to electrophiles Free Radical Biol Med 36, 1208–1213 60 Xu C, Li CY & Kong AN (2005) Induction of phase I, II and III drug metabolism ⁄ transport by xenobiotics Arch Pharm Res 28, 249–268 61 Davoine C, Douki T, Iacazio G, Montillet JL & Trian` taphylides C (2005) Conjugation of keto fatty acids to glutathione in plant tissues Characterization and quantification by HPLC-tandem mass spectrometry Anal Chem 77, 7366–7372 62 Davoine C, Falletti O, Douki T, Iacazio G, Ennar N, ` Montillet JL & Triantaphylides C (2006) Adducts of oxylipin electrophiles to glutathione reflect a 13 specificity of the downstream lipoxygenase pathway in the tobacco hypersensitive response Plant Physiol 140, 1484–1493 63 Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ & Berger S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis Plant Cell 20, 768–785 ` ´ 64 Mene-Saffrane L, Davoine C, Stolz S, Majcherczyk P & Farmer EE (2007) Genetic removal of tri-unsaturated fatty acids suppresses developmental and molecular phenotypes of an Arabidopsis tocopherol-deficient mutant Whole-body mapping of malondialdehyde pools in a complex eukaryote J Biol Chem 282, 35749– 35756 ´ 65 Vollenweider S, Weber H, Stolz S, Chetelat A & Farmer EE (2000) Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves Plant J 24, 467–476 ´ 66 Weber H, Chetelat A, Reymond P & Farmer EE (2004) Selective and powerful stress gene expression in Arabid- OPDA triggered responses in plants 67 68 69 70 71 72 73 74 75 76 77 78 79 opsis in response to malondialdehyde Plant J 37, 877– 888 Thoma I, Loeffler C, Sinha AK, Gupta M, Krischke M, Steffan B, Roitsch T & Mueller MJ (2003) Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants Plant J 34, 363–375 Mueller MJ (2004) Archetype signals in plants: the phytoprostanes Curr Opin Plant Biol 7, 441–448 ` ´ Mueller MJ, Mene-Saffrane L, Grun C, Karg K & Farmer EE (2006) Oxylipin analysis methods Plant J 45, 472–489 ` ´ ´ Mene-Saffrane L, Dubugnon L, Chetelat A, Stolz S, Gouhier-Darimont C & Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis J Biol Chem 284, 1702–1708 ` ´ Sattler SE, Mene-Saffrane L, Farmer EE, Krischke M, Mueller MJ & DellaPenna D (2006) Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants Plant Cell 18, 3706–3720 Dueckershoff K, Mueller S, Mueller MJ & Reinders J (2008) Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana Biochim Biophys Acta 1784, 1975–1985 Straus DS & Glass CK (2001) Cyclopentenone prostaglandins: new insights on biological activities and cellular targets Med Res Rev 21, 185–210 Bowers RC, Hevko J, Henson PM & Murphy RC (2000) A novel glutathione containing eicosanoid (FOG7) chemotactic for human granulocytes J Biol Chem 275, 29931–29934 ´ Cernuda-Morollon E, Pineda-Molina E, Canada FJ & ˜ ´ Perez-Sala D (2001) 15-Deoxy-D12,14-prostaglandin J2 inhibition of NF-jB–DNA binding through covalent modification of the p50 subunit J Biol Chem 276, 35530–35536 ´ ´ Perez-Sala D, Cernuda-Morollon E & Canada FJ ˜ (2003) Molecular basis for the direct inhibition of AP-1 DNA binding by 15-deoxy-D12,14-prostaglandin J2 J Biol Chem 278, 51251–51260 Shiraki T, Kamiya N, Shiki S, Kodama TS, Kakizuka A & Jingami H (2005) a,b-Unsaturated ketone is a core moiety of natural ligands for covalent binding to peroxisome proliferator-activated receptor c J Biol Chem 280, 14145–14153 Stintzi A, Weber H, Reymond P, Browse J & Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones Proc Natl Acad Sci USA 98, 12837–12842 Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T et al (2005) 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4703 OPDA triggered responses in plants 80 81 82 83 84 85 86 87 88 89 90 C Bottcher and S Pollmann ă role in wound-induced gene expression in Arabidopsis Plant Physiol 139, 1268–1283 Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC & Pieterse CM (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation Plant Physiol 147, 1358–1368 Koornneef A & Pieterse CM (2008) Cross talk in defense signaling Plant Physiol 146, 839–844 Mou Z, Fan W & Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes Cell 113, 935–944 ´ Despres C, DeLong C, Glaze S, Liu E & Fobert PR (2000) The Arabidopsis NPR1 ⁄ NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors Plant Cell 12, 279–290 Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J & Klessig DF (2000) NPR1 differentially interacts with members of the TGA ⁄ OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid Mol Plant Microbe Interact 13, 191–202 Ribot C, Zimmerli C, Farmer EE, Reymond P & Poirier Y (2008) Induction of the Arabidopsis PHO1;H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1dependent pathway Plant Physiol 147, 696–706 Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone Annu Rev Plant Biol 60, 183–205 Shibata T, Yamada T, Ishii T, Kumazawa S, Nakamura H, Masutani H, Yodoi J & Uchida K (2003) Thioredoxin as a molecular target of cyclopentenone prostaglandins J Biol Chem 278, 26046–26054 Wagner U, Edwards R, Dixon DP & Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family Plant Mol Biol 49, 515–532 Bakan B, Hamberg M, Perrocheau L, Maume D, Rogniaux H, Tranquet O, Rondeau C, Blein JP, Ponchet M & Marion D (2006) Specific adduction of plant lipid transfer protein by an allene oxide generated by 9-lipoxygenase and allene oxide synthase J Biol Chem 281, 38981–38988 Stelmach BA, Muller A, Hennig P, Gebhardt S, ă Schubert-Zsilavecz M & Weiler EW (2001) A novel class of oxylipins, sn1-O-(12-oxophytodienoyl)-sn2-O- 4704 91 92 93 94 95 96 97 98 99 100 (hexadecatrienoyl)-monogalactosyl diglyceride, from Arabidopsis thaliana J Biol Chem 276, 12832–12838 Hisamatsu Y, Goto N, Hasegawa K & Shigemori H (2003) Arabidopsides A and B, two new oxylipins from Arabidopsis thaliana Tetrahedron Lett 44, 5553– 5556 Hisamatsu Y, Goto N, Sekiguchi M, Hasegawa K & Shigemori H (2005) Oxylipins arabidopsides C and D from Arabidopsis thaliana J Nat Prod 68, 600–603 Andersson MX, Hamberg M, Kourtchenko O, ˚ Brunnstrom A, McPhail KL, Gerwick WH, Gobel C, ă ă Feussner I & Ellerstrom M (2006) Oxylipin proling of ă the hypersensitive response in Arabidopsis thaliana Formation of a novel oxo-phytodienoic acid-containing galactolipid, arabidopside E J Biol Chem 281, 31528– 31537 Nakajyo H, Hisamatsu Y, Sekiguchi M, Goto N, Hasegawa K & Shigemori H (2006) Arabidopside F, a new oxylipin from Arabidopsis thaliana Heterocycles 69, 295–301 Kourtchenko O, Andersson MX, Hamberg M, Brunnstrom A, Gobel C, McPhail KL, Gerwick WH, ă ă Feussner I & Ellerstrom M (2007) Oxo-phytodienoic ă acid-containing galactolipids in Arabidopsis: jasmonate signaling dependence Plant Physiol 145, 1658–1669 Bottcher C (2007) Studies on the biology of free and ă esteried phytodienoic acids Doctoral thesis, Ruhr-University Bochum, Germany Buseman CM, Tamura P, Sparks AA, Baughman EJ, Maatta S, Zhao J, Roth MR, Esch SW, Shah J, Williams TD et al (2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic acid and dinor-oxophytodienoic acid in Arabidopsis leaves Plant Physiol 142, 28–39 Hisamatsu Y, Goto N, Hasegawa K & Shigemori H (2006) Senescence-promoting effect of arabidopside A Z Naturforsch 61, 363–366 Bottcher C & Weiler EW (2007) cyclo-Oxylipin-galacă tolipids in plants: occurrence and dynamics Planta 226, 629–637 Yang W, Devaiah SP, Pan X, Isaac G, Welti R & Wang X (2007) AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea J Biol Chem 282, 18116– 18128 FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS ... arachidonic acid, a fourfold unsaturated C20 fatty acid, and have pivotal functions in the inflammatory process, in general reactions to infections and in allergic responses [9] By contrast, phytooxylipins... Weber H, Stolz S, Chetelat A & Farmer EE (2000) Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves Plant J 24,... work on phytoprostanes allow for hypotheses in which bioactive plant RES act as Michael acceptors, thereby adding not only to GSH, but also directly to enzymes and transcription factors OPDA: