Jasmonates in flower and seed development

Biochimie 95 (2013) 79e85

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Review

Jasmonates in flower and seed development Claus Wasternack a, *, Susanne Forner b, Miroslav Strnad c, Bettina Hause b a

Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, D-06120 Halle (Saale), Germany Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3, D-06120 Halle (Saale), Germany c Centre of the Region Haná for Biotechnological and Agricultural Research, Palacký University, Olomouc, Czech Republic b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 27 March 2012 Accepted 4 June 2012 Available online 13 June 2012

Jasmonates are ubiquitously occurring lipid-derived signaling compounds active in plant development and plant responses to biotic and abiotic stresses. Upon environmental stimuli jasmonates are formed and accumulate transiently. During flower and seed development, jasmonic acid (JA) and a remarkable number of different metabolites accumulate organ- and tissue specifically. The accumulation is accompanied with expression of jasmonate-inducible genes. Among these genes there are defense genes and developmentally regulated genes. The profile of jasmonate compounds in flowers and seeds covers active signaling molecules such as JA, its precursor 12-oxophytodienoic acid (OPDA) and amino acid conjugates such as JA-Ile, but also inactive signaling molecules occur such as 12-hydroxy-JA and its sulfated derivative. These latter compounds can occur at several orders of magnitude higher level than JA. Metabolic conversion of JA and JA-Ile to hydroxylated compounds seems to inactivate JA signaling, but also specific functions of jasmonates in flower and seed development were detected. In tomato OPDA is involved in embryo development. Occurrence of jasmonates, expression of JA-inducible genes and JAdependent processes in flower and seed development will be discussed. Ó 2012 Elsevier Masson SAS. All rights reserved.

Keywords: Jasmonates Flowers Seeds Jasmonate-induced genes Defense Development

1. Introduction Jasmonic acid (JA) and its metabolites collectively called jasmonates are lipid-derived signaling molecules. They are active in plant development and plant stress responses together with other plant hormones. Among developmental processes jasmonates modulate root growth, flower development, senescence and tendril coiling [1]. Jasmonates increase upon biotic stress such as herbivory or pathogen attack and upon abiotic stress such as wounding, ozone or UV light [2e4]. The rise in jasmonates leads to dramatic reprogramming of expression of genes involved in flower development [5], defense against herbivores [6,7] or formation of secondary metabolites [8e10] and other metabolic pathways [11]. The biosynthesis of jasmonates is initiated by the release of alinolenic acid (a-LeA) (18:3) from plastid membranes by a galactolipase. Upon oxygenation by a 13-lipoxygenase (13-LOX), the 13(S)-hydroperoxyoctadecatrienoic acid (13(S)-HPOT) is converted to an epoxide by a 13-allene oxide synthase (AOS) and cyclized to the cyclopentenone (cis)-12-oxophytodienoic acid (OPDA) by an

* Corresponding author. Tel.: þ49 345 5582 1210; fax: þ49 345 5582 1219. E-mail addresses: [email protected], [email protected] (C. Wasternack), [email protected] (S. Forner), [email protected] (M. Strnad), [email protected] (B. Hause). 0300-9084/$ e see front matter Ó 2012 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.biochi.2012.06.005

allene oxide cyclase (AOC) [4,12]. In this step the enantiomeric structure of the naturally occurring (þ)-7-iso-JA ((3R,7S)-JA) is established. Galactolipase, 13-LOX, AOS, and AOC are located in plastids. The subsequent reduction of the cyclopentenone ring by an OPDA reductase (OPR3) and three cycles of b-oxidation of the carboxylic acid side chain by fatty acid b-oxidation enzymes take place in peroxisomes. The final product (þ)-7-iso-JA may equilibrate to the more stable ()-JA ((3R,7R)-JA). Mechanistic insights into catalysis of JA biosynthesis enzymes were found after crystallization of 13-LOX, 13-AOS, AOC, OPR3 and ACX1 [12]. Mutants in JA biosynthesis and signaling have been contributed notably in elucidating jasmonate-dependent processes [13,14]. Most prominent examples for mutants of JA biosynthesis are the triple mutant fad3e2fad7e2fad8 which is affected in formation of a-LeA and opr3 affected in the reduction of OPDA by OPR3. The opr3 mutant is JA-deficient but can form OPDA, whereas the mutant fad3e2fad7e2fad8 lacks JA and OPDA. A constitutive JA response occurs in cev1, in which a gene encoding CES3, a member of the cellulose synthase complex, is mutated. Among the numerous mutants with reduced or even lack of sensitivity to JA, coi1 is the most prominent member. CORONATINE (a molecular mimic of jasmonates) INSENSITIVE protein COI1 is an F-box protein [15], a central component of jasmonate perception (cf. below). Characteristic phenotypes of JA deficiency or insensitivity are reduced root growth inhibition,

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male sterility (Arabidopsis), female sterility (tomato), enhanced sensitivity to necrotrophic pathogens or diminished synthesis of secondary compounds such as anthocyanins. In long-term processes, such as development or long-lasting and repeatedly performed wounding, JA biosynthesis is regulated by a positive feedback loop [4,16,17]. All genes encoding JA biosynthesis enzymes are JA-inducible, and JA-deficient mutants show decreased expression of those genes such as AOC [4,17]. Numerous studies showed that JA formation takes place very rapidly within some minutes after an external stimulus such as wounding [18,19]. All biosynthetic enzymes analyzed so far (LOX, AOS and AOC) occur constitutively and abundantly in leaves. Following a stimulus, JA is formed then upon release of a-LeA, the substrate of JA biosynthesis. Consistently, transgenic lines over-expressing AOS or AOC did not show increased JA levels without external stimuli [20,21]. These facts clearly indicate that substrate availability is a regulatory factor of JA biosynthesis [4]. A putative enzyme activity regulation, however, is poorly understood. Another factor of regulation of JA biosynthesis is given by cell- and tissue-specific occurrence of JA biosynthetic enzymes [22], thereby attributing to localized generation of JA, e.g. during wounding [3,23]. In the last couple of years several breakthroughs improved our knowledge on regulation of JA signaling and therefore also JA biosynthesis: (i) jasmonate-ZIM-domain (JAZ) proteins were discovered and identified as repressors of JA-induced gene expression [24,25]; (ii) (þ)-7-iso-JA-Ile was identified as the endogenous bioactive jasmonate [26]; (iii) COI1 of Arabidopsis was identified as constituent of the jasmonate co-receptor complex [27]; (iv) The COI1eJAZ co-receptor complex was crystallized and shown to be potentiated in jasmonate perception by inositol5-phosphate [28]; (v) NINJA was shown to connect the co-repressor TOPLESS to JAZ proteins [29]; (vi) Similar signaling modules are components in regulation of gene expression of jasmonate-, gibberellic acid-, ABA- and auxin-induced processes. They include transcription factors, transcriptional repressors, and a co-receptor complex connecting the repressor and the SCF-complex upon hormone binding [30e32]. JA-Ile is the most bioactive jasmonate compound [26]. Numerous other JA metabolites have been identified being formed by decarboxylation, glucosylation, or hydroxylation of the pentenyl side chain or by sulfation of the hydroxylated derivatives [4,12]. Some of these compounds such as 12-OH-JA were identified to be inactive suggesting a switch off in JA signaling by metabolic conversion [33]. There are, however, distinct developmental processes such as tuber formation or nyctinastic leaf movement, where these metabolites have biological activity [34,35]. Here, we will discuss occurrence and putative functions of jasmonates in flower and seed development. After a descriptive overview on various jasmonate compounds detected in flowers and seeds, jasmonate-responsive gene expression in flower organs will be discussed in terms of putative functions. A new example on OPDA specific effects will be given by describing its role in embryo development of tomato. 2. Occurrence of jasmonate and its derivatives in flowers and seeds Although there is no systematic study, the available data indicate that the content and number of JA compounds can differ

extremely in various plants and during flower and seed development. In monocotyledonous plants such as Hordeum vulgare OPDA, JA, 12-OH-JA, the sulfated derivative 12-HSO4-JA and the glucoside 12-O-Glc-JA occur with a basal level of about 150 to 2.100 pmol g1 FW in green and white caryopses, but in Zea mays the corresponding levels of these compounds range from 1.700 to 94.500 pmol g1 FW in tassels, silks and pollen [33]. Similarly, high levels were found in the pericarp of Glycine max and Vicia faba, whereas the pericarp of Cucumis sativa contains only residual amounts of these compounds. The dominant occurrence of OPDA compared to JA may indicate its role during flower and seed development as recently shown for tomato flowers and seeds [36], (cf. chapter 5). The extremely high levels of 12-OH-JA, 12-HSO4-JA and 12-O-Glc-JA in some flowers organs may indicate a role as an inactive or storage form of JA [33]. In the early days of JA research numerous JA compounds were identified in flower and seed tissues without any hint on putative functions (Table 1). These data go back to first identification of JA and JA-Me as odorant constituents of flowers of Jasminum grandiflorum [37]. First physiological effects of jasmonates were shown to be senescence promotion in several plant species [38] and pericarp growth inhibition in V. faba [39]. Using the present knowledge on the various facets in JA signaling generated by metabolic conversion, the data on occurrence of the various JA compounds may help to ask for distinct roles in different organs and tissues. 3. JA biosynthesis in flower tissues Fundamental contributions were done on involvement of JA in flower development by phenotype analyses of mutants. In Arabidopsis several mutants of JA biosynthesis are male sterile due to delayed anther development and/or reduced filament elongation (cf. reviews in [13,14]). Among them are all JA-deficient mutants, such as dad1 (defective in a phospholipase A1), fad3e2fad7e2fad8

Table 1 Early detection of jasmonates in flowers of various mono- and dicotyledonous plant species. Species

Organ/tissue

Petunia hybrida

Pollen

Compound

N-(()-jasmonoyl) -tyramin Pinus mugo Pollen N-(()-jasmonoyl) -(S)-iso-leucine N-(7-iso-cucurbinoyl) -(S)-iso-leucine Juglans regia Female flowers ()-JA 6-epi-7-iso-cucurbic acid 6-epi-cucurbic acid Cymbidium faberi Flowers ()-JA-Me (þ)-7-iso-JA-Me Jasminum grandiflorum Flowers cis-jasmone (þ/)-JA Cymbidium kanran Flowers JA-Me (þ)-7-iso-JA-Me Vicia faba Flowers ()-JA ()-JA-Me (þ)-7-iso-JA Cattleya luteola Flowers cis-jasmone Equisetum sylvaticum Fertile fronds 6-epi-7-iso-cucurbic acid V. faba Flowers N-(()-jasmonoyl) -S-tryptophan N-((þ)-cucurbinoyl) -S-tryptophan Flowers JA-Me Aglaia odorata Camelliia sinensis Anthers, pollen (þ/)-JA (þ/)-JA-Me Phaseolus vulgaris and Immature pericarp (þ/)-JA-Me other Fabaceae

Reference [76] [77]

[78]

[79] [37,80] [81] [82]

[83] [84] [85]

[86] [87] [88]

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(defective in an u-7-fatty acid desaturase), dde2-2 (an AOS mutant), dd1 and opr3 (both of them defective in OPR3), and aim1 (mutated in MFP1). In case of the 13-LOXs, which are encoded by a family of four genes, only the lox3lox4 double mutant exhibited a male sterile phenotype [40]. Male sterility occurs also in the most prominent JA perception mutant affected in COI1 [15]. Interestingly, the mutant jai1 affected in the tomato homolog of COI1 is female sterile [41]. This points to different functions of the same hormone in flower development of different species. Surprisingly, the reproductive organs of the monoecious monocotyledonous plant Z. mays are determined JA-dependently due to the involvement of a JA biosynthesis enzyme [42]: Sex determination of the male organ, the tassels, requires TASSELSEED1, which is a LOX [13,42]. The involvement of JA biosynthesis genes in flower organ development is also suggested by expression studies for different flower organs (cf. data from www.genevestigator.ethz.ch) as well as by analyses of corresponding promoter activities. Here, GUS activities were recorded in different flower organs of Arabidopsis with AOS [43] and AOC promoter GUS line, respectively (Stenzel et al., in preparation). Involvement of JA-dependent transcriptions factors in stamen development was elucidated by transcription profiling [5]. Initial data obtained from JA-treated opr3 plants identified 13 transcriptions factors as key regulators of JA-dependent stamen development. Subsequently, five of them, MYB21, MYB24, MYB32, MYB108 and IAA19, were shown by genetic evidences to be involved in stamen and pollen maturation [5,44]. The factors MYB21 and MYB24 are active via proteineprotein interaction with JAZ proteins, the repressors of JA-dependent gene expression [45]. Recently, MYB21 and MYB24 were shown to be required also for gynoecium and petal growth [46]. Both transcription factors are expressed JAdependently. This regulation depends on intact auxin signaling by AUXIN RESPONSE FACTOR6 (ARF6) and ARF8. Both ARFs induce JA biosynthesis in filaments and the arf6-2arf8-3 flowers exhibit low JA-levels in filaments [47]. Obviously, petal and stamen growth are determined by a common regulatory network containing the JAdependent transcription factors MYB21 and MYB24 as well as the auxin-dependent transcription factors ARF6 and ARF8 [46]. Another player in JA-regulated flower organ development is AGAMOUS. This central regulator in reproductive organ development is encoded by a floral homeotic gene. The regulation is mediated by expression of JA biosynthesis genes, such as that encoding DAD1, the a-LeA-generating galactolipase of Arabidopsis flowers. and by direct proteineprotein interaction of DAD1 and AGAMOUS [48]. 4. JA-induced defense gene expressed in flower organs The organ-specific occurrence of jasmonates described in chapter 2 corresponds at least partially to organ-specific expression of JA biosynthesis genes. In case of tomato abundant occurrence of AOC protein in ovules correlates to high levels of jasmonates in pistils [22]. A similar correlation was found upon large scale expression analysis in Nicotiana tabacum stigmas which led to establishment of the TOBEST database [49]. Due to the positive feedback loop in JA formation, expression of JA biosynthesis genes might depend on a corresponding activity of transcription factors in the same organ. As described above, MYB21 and MYB24 are examples, how JA levels and expression of JA biosynthesis genes are linked. However, in case of JA biosynthesis genes a JA-independent, developmentally regulated expression seems to occur additionally, since AOC protein was clearly detectable in ovules of the JAinsensitive mutant jai1 of tomato [36]. Nevertheless, a link between organ-specific JA formation and JAinducible defense gene expression can be expected. Indeed,

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numerous JA-inducible defense genes are up-regulated in organs carrying elevated JA levels. Among them are those encoding Proteinase Inhibitor2 (PIN2) [41,50], Threonine Deaminase [51], Leucine Aminopeptidase [52,53], Defensins [54] or Thionins [53]. The schematic picture shown in Fig. 1 illustrates some basic aspects for tomato flowers: The important enzyme in JA biosynthesis occurs abundantly in ovules [22] which correspond to AOC promoter activity in ovules [55]. Due to the preferential expression of a Cell Wall Invertase (LIN5) in gynoecia of tomato [56], hexoses might be generated locally. Indeed, this organ-specific increase in hexoses was detected [57] and reflects the sink properties of ovules. A rise in glucose may attribute to an organ-specific increase in expression of AOS and AOC, which both are glucose-inducible [22,58]. Subsequently, increase in OPDA and JA seems to occur which was detected for pistils [22]. Consequently, JA-inducible defense genes mentioned above might be expressed. Such regulatory circuit might attribute to an increased defense in an organ, which would be highly attractive to biotic stressors due to increased sugar levels. Indeed, there are not many herbivores known to infest flower organs such as ovules. This is presumable caused by increased PIN2 expression [36]. PIN2 is known to attack herbivores by inhibition of protein digestion in the gut [59]. Beside the link between JA biosynthesis and defense gene expression observed in tomato flowers before anthesis, another scenario could be recently described for JA biosynthesis and tomato embryo development [36]. 5. Role of cis-OPDA in tomato embryo development The JA conjugate (þ)-7-iso-JA-Ile is the most active ligand of COIeJAZ co-receptor complex [26e28]. The JA-precursor OPDA does not bind to this receptor, but it has individual JA- and COI1independent signaling properties [60e62]. Although there is no mechanistic explanation so far on OPDA perception, examples increase on JA- and COI1-independent signaling by OPDA. A most recent scenario was given for embryo development in tomato [36]. Here, a similar phenotype of female sterile jai1 plants and 35S::SlAOC-RNAi lines was observed suggesting that a compound downstream of the AOC catalyzed step is required for proper embryo development. Any proof by analysis of the 35S::SlAOC-RNAi lines was hampered by their low seed set. Interestingly, the spr2 mutant affected in the u-7-fatty acid desaturase showed also a defective embryo development leading to aborted embryos accompanied by a shrunken endosperm. In contrast, the acx1 mutant affected in the acyl-CoA oxidase 1 showed normal seed development as demonstrated for embryos in the curled cotyledon stage, which were similar to those of the wild type (Fig. 2). Since ACX1 catalyzes a step downstream of OPDA, this compound or a related metabolite was assumed to be required for proper embryo development. Surprisingly, OPDA accumulated predominantly during embryo development in the seed coat, whereas downstream compounds such as JA and 12-OH-JA appeared only in residual amounts in the seed coat, endosperm and embryo, and the acx1 mutant seeds exhibited as expected an OPDA level higher than wild type seeds. In spr2 seeds an enhanced programmed cell death was observed within seed coat and endosperm tissues by the TUNEL assay, suggesting that both tissues are affected by diminished OPDA levels. Due to its high level in the seed coat of wild type plants and the ability of acx1 to produce OPDA, this compound was assumed to be an important regulator of embryo development. There is, however, a residual amount of JA/JA-Ile in the acx1 seeds which might be sufficient for proper embryo development. To distinguish between OPDA and JA/JA-Ile, the jai1 mutant was used. This mutant is JA-insensitive, but able to perceive OPDA [28,41]. Indeed, jai1 plants repeatedly wounded in a time window of embryo development showed partially normalized embryo

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Fig. 1. In tomato flower buds ovules exhibit abundant accumulation of AOC protein which is glucose-inducible. As a sink tissue ovules may accumulate glucose which leads to expression of AOS and AOC and finally to accumulation of OPDA and JA. In parallel, expression of defense genes, such as PIN2 was detected in ovules [36], which correlates with a high defense status of flower organs against herbivores and pathogens. Additionally, effects of OPDA and JA on fertility and seed development were observed. A. Flowers of the cultivar Micro-Tom, B. Dissected pistil, C. Section through an ovary, D. AOC immunostain of a cross section of ovary showing labeling of ovules.

development and elevated OPDA levels in fruits compared to fruits of unwounded plants. In the first view, this rise in OPDA seems to contradict to the well-known fact that genes encoding enzymes of JA biosynthesis are regulated in a COI1- and JA-dependent manner [63]. There seems to occur, however, a residual COI1-independent JA formation, since AOC was detected immunocytochemically in ovules of jai1 [36]. In summary, the available data support a role of seed coat-generated OPDA in embryo development of tomato. Among putative mechanisms of OPDA action, an effect of OPDA on carbon availability is one scenario. The JA-inducible cell wall invertase LIN5 is preferentially expressed in gynoecia [56], but LIN5-silenced lines show lower seed set, oxylipin content and hexose levels [57]. Correspondingly, silencing of the cell wall invertase inhibitor INVINH1, which is usually co-expressed with LIN5, led to restored invertase activity and hexose generation [64]. INVINH1 is OPDA-dependently suppressed [62] allowing to draw the following hypothesis: seed coat-generated OPDA may downregulate INVINH1 expression, thereby allowing LIN5 activity which generates hexose for proper embryo development. 6. Conclusions

Fig. 2. Embryo formation in tomato wild type, spr2 (a-LeA-, OPDA-, and JA-deficient) and acx1a (OPDA-accumulating but JA-deficient). Four weeks after fertilization, embryos of the curled cotyledon stage are visible in fruits of the wild type and the acx1 mutant, whereas spr2 embryos show an early arrest in development. The phenotype suggests that OPDA or a related metabolite is sufficient for proper embryo development. This hypothesis was substantiated by genetic and biochemical data [36]. Bars ¼ 1 mm.

In the last couple of years the role of JA biosynthesis and JA signaling for flower development has been elucidated in much more detail. The mutants of JA biosynthesis and JA signaling described above for Arabidopsis are male sterile [1,13,14], whereas the JAinsensitive tomato mutant jai1 is female sterile [41]. Due to the fact that jai1 pollen are viable and induce normal seed set when crossed with wild type pistils, JA perception and downstream JA signaling are not required for pollen development of tomato which is in contrast to Arabidopsis. Such species-specific differences in action

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of JA ask for putative evolution. Obviously, we have to assume a conservative function in defense and a later evolved specific function, e.g. in reproduction [65]. Such a scenario is reminiscent to the metabolic diversity among evolution of secondary compounds (cf. special issue of Phytochemistry 70, 2009 [66]). Beside the roles of JA and other oxylipins in flower development elucidated so far, there is an ongoing increase in new research areas related to JA and flower and seed development: (i) In addition to the COI1- and JA-independent action of OPDA described here for embryo development, there are several new examples on such OPDA specific roles. In Arabidopsis, the inhibition of seed germination was assumed for a long time to be mediated by JA. However, recent genetic and biochemical evidences showed that seed germination is regulated by endogenously accumulated OPDA in a COI1-independent manner [67,68]. (ii) Role of JA and other oxylipins in light perception and signaling is a new aspect [69,70]. (iii) Further examples on tissue-specific occurrence of jasmonates and expression of JA-dependent gene activation will increase our knowledge on action of jasmonates in flower development. (iv) Beside the switch off in wound-induced JA signaling by hydroxylation of JA to 12-OH-JA [33], hydroxylation and carboxylation of JA-Ile in the pentenyl side chain have been detected recently by cloning of the corresponding CYP450 enzymes and could be characterized as an inactivation of JA-Ile signaling [71,72]. Consequently, we have to assume that metabolic conversion of jasmonates is a mechanism for fine tuning of JA signaling even in flowers. (v) JA-dependent formation of secondary compounds such as anthocyanins, glycosinolates, and flavonoids, and JAdependent release of flower volatiles and nectar secretion occur. Several of these aspects are of consequence for crop quality, protection against pathogens and chilling injury as well as for harvest ability [73]. (vi) JA-dependent balances between defense and flowering [69] and between defense and growth suppression [74] have to be regarded. Such a role of JA in orchestrating plant growth, defense and reproduction will illustrate its activity in an ecological context [75].

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