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Keywords:

  • 12-oxo-phytodienoic acid;
  • cyclo-oxylipin-galactolipids;
  • environmental stress;
  • jasmonates;
  • jasmonic acid;
  • mechanotransduction;
  • oxylipins;
  • phytoprostanes;
  • plant stress responses;
  • transcriptional regulation

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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.


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

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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 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 α-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, α-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 β-oxidation, is deemed to be basically uncovered with respect to the enzymes involved (for a review see Ref. [7]).

image

Figure 1.  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.

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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 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 α-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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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 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 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 μm) 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 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.

image

Figure 2.  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

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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 β-d-glucopyranosyl 12-hydroxyjasmonate, may at least contribute to this distinct type of plant movement. In particular, nyctinastic leaf closing is mediated by potassium β-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 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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 α,β-unsaturated keto or epoxy functions can behave like reactive electrophilic species (RES) towards cellular nucleophiles [57]. In this regard, α,β-unsaturated keto groups can participate in nucleophilic Michael additions in which carbanions are added to α,β-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 α-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 3 fatty acids, in particular α-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 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 α,β-unsaturated carbonyl groups [73]. Hydroperoxy arachidonic acids, like leukotriene C4 and 5-oxo-7-glutathionyl-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-κB), c-Jun or peroxisome proliferator-activated receptor (PPARγ) [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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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 COI1-dependent genes were induced in wounded or OPDA-treated opr3 plants, but both treatments activated the transcription of several COI1-independent genes, which were not influenced 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 indole-3-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 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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. Böttcher et al., unpublished 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 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 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

Cyclic oxylipins do 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 lipid-bound 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 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.

image

Figure 3.  Structures of the currently identified cyclo-oxylipin-galactolipids from Arabidopsis thaliana.

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Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Physiological processes mediated by OPDA
  5. A proposed mechanism of OPDA action
  6. OPDA: an independent regulator of gene expression
  7. Regulating the pool of free OPDA by conjugation
  8. OPDA can be released from cyclo-oxylipin-galactolipids
  9. Conclusions
  10. Acknowledgements
  11. References