Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development

Goetz, Stephan J.; Hellwege, Anja; Stenzel, Irene; Kutter, Claudia; Hauptmann, Valeska; Forner, Susanne; McCaig, Bonnie C.; Hause, Gerd; Miersch, Otto; Wasternack, Claus; Hause, Bettina

doi:10.1104/pp.111.192658

Cited by 88 publications

(70 citation statements)

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“…After successful fertilization, NO and JA are likely also important during embryo development (Supplemental Fig. S9; Goetz et al, 2012) and defense (Bosch et al, 2014), as indicated by recent studies in tomato (Solanum lycopersicum). Therefore, it is conceivable that our findings have important implications for other plant species and conditions in which NO and/or JA act as signaling components: in the case of peroxisomal NO during abiotic stress in roots (Corpas et al, 2009;Corpas and Barroso, 2014a) and in the case of JA during herbivory/wounding or plant-pathogen interactions.…”

Section: Discussionmentioning

confidence: 96%

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana

et al. 2016

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We studied the localization of 6-phosphogluconate dehydrogenase (PGD) isoforms of Arabidopsis (Arabidopsis thaliana). Similar polypeptide lengths of PGD1, PGD2, and PGD3 obscured which isoform may represent the cytosolic and/or plastidic enzyme plus whether PGD2 with a peroxisomal targeting motif also might target plastids. Reporter-fusion analyses in protoplasts revealed that, with a free N terminus, PGD1 and PGD3 accumulate in the cytosol and chloroplasts, whereas PGD2 remains in the cytosol. Mutagenesis of a conserved second ATG enhanced the plastidic localization of PGD1 and PGD3 but not PGD2. Amino-terminal deletions of PGD2 fusions with a free C terminus resulted in peroxisomal import after dimerization, and PGD2 could be immunodetected in purified peroxisomes. Repeated selfing of pgd2 transfer (T-)DNA alleles yielded no homozygous mutants, although siliques and seeds of heterozygous plants developed normally. Detailed analyses of the C-terminally truncated PGD2-1 protein showed that peroxisomal import and catalytic activity are abolished. Reciprocal backcrosses of pgd2-1 suggested that missing PGD activity in peroxisomes primarily affects the male gametophyte. Tetrad analyses in the quartet1-2 background revealed that pgd2-1 pollen is vital and in vitro germination normal, but pollen tube growth inside stylar tissues appeared less directed. Mutual gametophytic sterility was overcome by complementation with a genomic construct but not with a version lacking the first ATG. These analyses showed that peroxisomal PGD2 activity is required for guided growth of the male gametophytes and pollen tube-ovule interaction. Our report finally demonstrates an essential role of oxidative pentose-phosphate pathway reactions in peroxisomes, likely needed to sustain critical levels of nitric oxide and/or jasmonic acid, whose biosynthesis both depend on NADPH provision.

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Section: Discussionmentioning

confidence: 96%

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana

et al. 2016

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“…The above described embryo phenotype of jai1 flowers could be partially rescued by endogenously formed OPDA in repeatedly wounded plants compared with un-wounded plants. 25 All these data suggest a COI1-independent role of seed coat-generated OPDA in embryo development of tomato.…”

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confidence: 88%

“…Indeed, OPDA was the dominant compound in the seed coat of wild type seed and accumulated in the acx1 seeds. 25 Increased programmed cell death (PCD) monitored by the TUNEL assay was observed in the seed coat and endosperm of spr2 seeds compared with that of wild type seeds. To proof whether OPDA was the essential compound for embryo development, a rescue of the embryo phenotype of spr2 seed was tried by OPDA treatment.…”

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Another JA/COI1-independent role of OPDA detected in tomato embryo development

Wasternack

Goetz

Hellwege

et al. 2012

Plant Signaling & Behavior

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(+)-7-iso-jasmonoyl isoleucine, the bioactive JA, is involved in most JA-dependent processes mediated by the F-box protein COI1 in a proteasome-dependent manner. However, there is an increasing number of examples, where the precursor of JA biosynthesis, cis-(+)-12-oxophytodienoic acid (OPDA) is active in a JA/COI1-independent manner. Here, we discuss those OPDA-dependent processes, thereby giving emphasis on tomato embryo development. Recent data on seed coat-generated OPDA and its role in embryo development is discussed based on biochemical and genetic evidences.The plant hormone jasmonic acid (JA) was initially detected as its methyl ester in the essential oil of flowers of Jasminum grandiflorum.1 In the sixties and the seventies numerous additional jasmonate compounds were detected preferentially in flowers.2 In the last three decades hydroxylated, glucosylated, sulphated, decarboxylated and carboxylated derivatives as well as JA amino acid conjugates have been identified as plant constituents. Upon wounding there is a rapid accumulation of JA, JA-Ile within some minutes, followed by accumulation of their hydroxylated, carboxylated and glucosylated derivatives. [3][4][5] Some of these JA metabolites occur in flower organs and seeds up to three orders of magnitude higher levels than JA. 6 All Another JA/COI1-independent role of OPDA detected in tomato embryo development 9-11 This metabolic conversion of JA and JA-Ile, respectively, leads to compounds being biologically inactive in some processes such as wounding, where JA and JA-Ile are typically involved as signaling compounds. 6,9,11 In contrast, an O-glycosylated JA derivative is active in leaf movement, 12 and decarboxylated JA, called cis-jasmone, leads to expression of a specific set of genes different from those involved in JA-induced gene expression. 13All these aspects contribute to the questions whether or not the different JA compounds exhibit individual specificity in signaling and which of the metabolic conversion of JA or JA-Ile represents a "switch off" in its signaling cascade.In the last couple of years a similar question was already addressed for the precursor of JA, 12-oxophytodienoic acid (OPDA). Cis-(+)-OPDA is formed by the allene oxide cyclase (AOC)-catalyzed step of JA biosynthesis (Fig. 1) leading to establishment of that enantiomeric structure which is a feature of the naturally occurring JA.7,14 OPDA accumulates upon wounding of leaves usually to higher levels than JA and JA-Ile. 3,4,15 Moreover, a large portion of OPDA is esterified within lipid membranes to numerous compounds. 16,17 These compounds are called arabidopsides due to their exclusive occurrence in the 25 The AOC-catalyzed step in JA biosynthesis is required for OPDA and JA generation. Therefore, the flower phenotype of 35S::AOC-RNAi lines was assumed to be caused by any compound formed downstream of the AOC step. Due to the low seed set of these RNAi lines, however, OPDA and JA levels could not be analyzed.Interestingly, the tomato mutant spr2 has a delay in proper embr...

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“…20 Additionally, seed formation in tomato is regulated by OPDA. 21 Stress responses in JA-deficient but OPDA-containing lower plant species, such as Marchantia polymorpha, 22 Selaginella martensii 23 and Physcomitrella patens, 24 point to a signaling function of OPDA. These data correspond to a proteomic analysis of about 6.000 proteins in A. thaliana showing that nearly 5% of the wound-inducible proteins are synthesized JA-independently, that means they are induced COI1-independently.…”

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OPDA-Ile – a new JA-Ile-independent signal?

Wasternack

Hause

2016

Plant Signaling & Behavior

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Expression takes place for most of the jasmonic acid (JA)-induced genes in a COI1-dependent manner via perception of its conjugate JA-Ile in the SCF COI1 -JAZ co-receptor complex. There are, however, numerous genes and processes, which are preferentially induced COI1-independently by the precursor of JA, 12-oxophytodienoic acid (OPDA). After recent identification of the Ile-conjugate of OPDA, OPDA-Ile, biological activity of this compound could be unequivocally proven in terms of gene expression. Any interference of OPDA, JA, or JAIle in OPDA-Ile-induced gene expression could be excluded by using different genetic background. The data suggest individual signaling properties of OPDA-Ile. Future studies for analysis of an SCF COI1 -JAZ co-receptorindependent route of signaling are proposed. Ten years ago, the new family of JASMONATE ZIM DOMAIN (JAZ) proteins with 12 members was occasionally identified in Arabidopsis in 3 different labs. [1][2][3] This was a breakthrough in JA research, since JAZ proteins were characterized as repressors of JA-Ile-induced gene expression. With identification of these proteins, it became clear that JA-Ile is perceived by the SCF COI1 -JAZ co-receptor complex. Components of this complex are the F-box protein called CORONATINE INSENSI-TIVE 1 (COI1), the Skp1/Cullin/complex with E3 ubiquitin ligase activity and the targets of the F-box protein, the JAZ proteins. JAZ proteins repress in the absence of JA-Ile positively acting transcription factors (TFs), such as MYC2, which bind to JA responsive elements (G-boxes) in the promoters of JAIle-regulated genes. Upon stress or developmentally regulated processes, an increase in JA-Ile level occurs leading to its binding in the SCF COI1 -JAZ co-receptor complex followed by proteasomal degradation of JAZ. Consequently, the free, positively acting MYC2 can switch on JA-Ile-responsive gene expression. 4 This basic scenario could be explained mechanistically upon crystallization of the complex, where an inositol-pentakisphosphate (IP 5 ) activates JA-Ile binding. 5 Interaction of the F-box protein COI1 and one of the JAZ proteins requires the C-terminal jas domain of JAZ. 6 This interaction is promoted by JA-Ile. Among the various stereo-isomeric forms of JA-Ile, the (+)-7-iso-JA-Ile has the highest activity. 7 JA-Ile perception via the SCF COI1 -JAZ-co-receptor complex was confirmed in the last couple of years including identification of new co-repressors and adaptors (for reviews, see refs. [8][9][10] ).There is, however, one open question due to the structural specificity in binding of the ligand JA-Ile. Among 40 different jasmonate compounds the stereoisomer (+)-7-iso-JA-Ile, carrying a ring conformation similar to coronatine, was most active. 7 Even coronatine was 10-fold more active then JA-Ile, although this bacterial toxin does not occur in plants. For the methyl ester of JA, for 12-oxo-phytodienoic acid (OPDA, the precursor of JA biosynthesis), and for OPDA-Ile (Fig. 1) no detectable promotion of JAZ3-COI1 interaction was recorded...

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Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development

Cited by 88 publications

References 76 publications

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana

Another JA/COI1-independent role of OPDA detected in tomato embryo development

OPDA-Ile – a new JA-Ile-independent signal?

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