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An evolutionarily ancient Fatty Acid Desaturase is required for the synthesis of hexadecatrienoic acid, which is the main source of the bioactive jasmonate in Marchantia polymorpha

ABSTRACT: Jasmonates are fatty acid derived hormones that regulate multiple aspects of plant development, growth and stress responses. Bioactive jasmonates differ between vascular plants and bryophytes (using jasmonoyl-L-isoleucine; JA-Ile and dinor-12-oxo-10,15(Z)-phytodienoic acid; dn-OPDA, respectively), but bind an evolutionarily conserved COI1 receptor. Whilst the biosynthetic pathways of JA-Ile in the model vascular plant Arabidopsis thaliana have been elucidated, the details of dn-OPDA biosynthesis in bryophytes are still unclear. Here, we identify an ortholog of Arabidopsis Fatty Acid Desaturase 5 (AtFAD5) in the model liverwort Marchantia polymorpha and show that FAD5 function is ancient and conserved between species separated by more than 450 million years of independent evolution. Similar to AtFAD5, MpFAD5 is required for the synthesis of 7Z-hexadecenoic acid. Consequently, in Mpfad5 mutants the hexadecanoic pathway is blocked, the dn-OPDA levels almost completely depleted and normal chloroplast development is impaired. Our results demonstrate that the main source of dn-OPDA in Marchantia is the hexadecanoic pathway and the contribution of the octadecanoid pathway, i.e. from OPDA, is minimal. Remarkably, despite extremely low levels of the bioactive hormone (dn-OPDA), MpCOI1-mediated responses to wounding and insect feeding can still be activated in Mpfad5 mutants, suggesting that dn-OPDA is not the only bioactive jasmonate and COI1 ligand in Marchantia.

ORGANISM(S): Marchantia polymorpha

PROVIDER: GSE186451 | GEO | 2022/01/11

REPOSITORIES: GEO

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Ligand diversity guarantees full activation of the jasmonate pathway in Marchantia polymorpha (array)

Project description:In plants, jasmonate signalling regulates a wide range of processes from growth and develop-ment to defence responses and thermotolerance. Bioactive jasmonates, such as JA, JA-Ile, OPDA and dn-OPDA, are derived from C18- and C16- fatty acids (FAs), which are found ubiquitously in the plant kingdom. Bryophytes also contain long chain C20- and C22- FAs (LCFAs), which are absent in most vascular plants but are found in organisms of other king-doms, including mammals. The existence of bioactive jasmonates derived from LCFAs is cur-rently unknown. Here, we describe the identification of an OPDA-like molecule derived from a C20-FA in Marchantia polymorpha, which we term C20-OPDA. This molecule accumulates upon wounding, and when applied exogenously can activate known COI1-dependent and -independent jasmonate responses. Furthermore, we identify a dn-OPDA-like molecule (Δ4-dn-OPDA) deriving from C20-OPDA and demonstrate it to be a ligand of the jasmonate co-receptor (MpCOI1-MpJAZ) in Marchantia. By analysing mutants involved in the production of LCFAs, we elucidate the major biosynthetic pathway of C20-OPDA and Δ4-dn-OPDA. Moreover, using a double mutant compromised in the production of both Δ4-dn-OPDA and dn-OPDA, we demonstrate the additive nature of these molecules in the activation of jasmonate responses. Taken together, our data identify LCFAs as a source of bioactive jasmonates that are essential to plant plasticity and resilience.

2022-05-17 | GSE195838 | GEO

Ligand diversity guarantees full activation of the jasmonate pathway in Marchantia polymorpha (RNA-Seq)

2022-05-17 | GSE195837 | GEO

A single JAZ repressor controls the jasmonate pathway in Marchantia polymorpha

Project description:JAZ genes are negative regulators of jasmonate responses with a dual function as repressors of transcription factors and co-receptors, together with COI1, of the hormone jasmonoyl-isoleucine (JA-Ile). This family has been mainly studied in angiosperms, where high gene redundancy hinders the characterization of a complete depletion of JAZ function. Moreover, the recent discovery that JA-Ile is not the sole COI1/JAZ ligand in land plants, as dn-OPDA is the bioactive ligand in Marchantia polymorpha, underscores the importance of studying JAZ co-receptors in bryophytes. Here we exploited the low gene redundancy of the liverwort Marchantia polymorpha to characterize the function of the single MpJAZ in this early-divergent plant lineage. We demonstrate that MpJAZ is the ortholog of AtJAZ and acts as a repressor of dinor-OPDA responses in Marchantia. Mpjaz mutants show a dwarf phenotype and severe developmental defects related to growth inhibition, consistent with a constitutive activation of the dinor-OPDA pathway and the overaccumulation of both dinor-OPDA and its precursor OPDA. The expression of AtJAZ3 in Mpjaz complements MpJAZ repressor function, indicating that JAZ function is conserved across land plants. However, AtJAZ3 is unable to form co-receptor complexes with MpCOI1 and dn-OPDA, which evidences that the Jas domain, and not only COI1, determines ligand specificity.

2018-11-10 | GSE118149 | GEO

Ligand-receptor co-evolution shaped the jasmonate pathway in land plants

Project description:Jasmonoyl-isoleucine regulates defence, growth and developmental responses in eudicots. Bryophyte genomes have conserved sequences for all JA-Ile signalling pathway components, but in contrast to higher plants, the bioactive hormone has not been identified. We show that the JA-Ile receptor COI1 is functionally conserved in the bryophyte Marchantia polymorpha, but responds to a different ligand. Although Marchantia plants neither synthesize nor respond to JA-Ile, loss-of-function Mpcoi1 mutants have phenotypic defects reminiscent of COI1-dependent functions in Arabidopsis. AtCOI1 functionally complements Mpcoi1 mutation and confers JA-Ile responsiveness on M. polymorpha, as does a single amino acid substitution in MpCOI1 that switches ligand specificity. Mass spectrometry quantification of cyclopentenone derivatives, bioactivity analysis and COI1-ligand interaction assays pinpointed two isomers of the JA-Ile precursor dinor-OPDA (dinor-cis-OPDA and dinor-iso-OPDA) as the natural MpCOI1 ligands. Our results identify the ancestral jasmonate, confirm the functional conservation of its signalling pathway, and show that JA-Ile and COI1 emergence in higher plants from their ancestral counterparts required co-evolution of hormone biosynthetic complexity and receptor specificity.

2018-04-10 | GSE99727 | GEO

Rational design of a ligand-based antagonist of jasmonate perception

Project description:The phytohormone (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) is a major regulator of developmental and stress responses in plants. The perception of JA-Ile involves the formation of a ternary complex with the F-box protein COI1 and a member of the JAZ family of co-repressors, which leads to JAZ degradation. Coronatine (COR) is a bacterial phytotoxin that functionally mimics JA-Ile and interacts with the co-receptor COI1-JAZ complex with higher affinity than JA-Ile. Based on the crystal structure of the co-receptor, we designed ligand derivatives that spatially impede the interaction of the co-receptor proteins and, therefore, should act as competitive antagonists of COR or JA-Ile. One derivative, Coronatine O-methyloxime (COR-MO), shows a strong activity preventing COI-JAZ interaction and the subsequent JAZ degradation. COR-MO efficiently reverts the effects of JA-Ile or COR treatments on JA-mediated responses, such as anthocyanin accumulation, root-growth inhibition and gene expression in Arabidopsis plants. Moreover, it potentiates plant resistance preventing the effect of bacterially produced COR during Pseudomonas syringae infections in different plant species. In addition to the utility of COR-MO for Plant Biology research, our results underscore its biotechnological and agronomical potential for a safer and sustainable agriculture.

2014-06-20 | GSE56027 | GEO

Rational design of a ligand-based antagonist of jasmonate perception

2014-06-20 | E-GEOD-56027 | biostudies-arrayexpress

Jasmonic acid signaling and glutathione coordinate plant recovery from high light stress

Project description:High light (HL)-induced chloroplast retrograde signaling originates from the photosynthetic apparatus and regulates nuclear gene expression to enhance photoprotection and coordinate cell metabolism. Here, we analyzed the transcript profiles and accumulation of reactive oxygen species (ROS), stress hormones and small molecule antioxidants to investigate the signaling mechanisms operating under HL stress, and in particular during plant recovery (R) from stress under growth conditions. Exposure to HL for 15 min induced a number of singlet oxygen (1O2) and hydrogen peroxide (H2O2)-responsive genes and accumulation of an oxidative form of glutathione (GSSG) and ascorbate (DHA), the hallmarks of oxidative stress in cells. Prolonged exposure to HL resulted in accumulation of transcripts encoding oxylipin biosynthesis enzymes, leading to accumulation of 12-oxo-phytodienoic acid (OPDA) and jasmonic acid (JA). However, the expression of several JA-responsive genes, already induced by HL, peaked during the R-phase (R-sustained) together with accumulation of JA, reduced glutathione (GSH) and ascorbate (AsA), highlighting the critical role of JA signaling in restoring chloroplast redox balance following HL stress. The involvement of JA signaling in R-sustained gene expression was further confirmed by conducting experiments with JA receptor mutants (coi1). HL exposure of only 2 min was sufficient to induce some R-sustained genes, indicating rapid response of plants to changing light conditions. We propose that ROS production at HL induces the signaling cascade for early oxylipin biosynthesis and OPDA accumulation, while increased accumulation of JA in R-phase activates the genes that fully restore the glutathione metabolism, and ultimately allow recovery from short-term HL stress.

2024-10-15 | GSE277977 | GEO

The maize death acids, 10-oxo-11-phytoenoic acid and derivatives, are rapidly induced phytoalexins with multiple biological activities

Project description:Plant cellular damage promotes the interaction of lipoxygenases (LOX) with free fatty acids to yield 9- and 13-hydroperoxides which are further metabolized into diverse oxylipins. The enzymatic action of 13-LOX on linolenic acid enables production of 12-oxo-phytodienoic acid (12-OPDA) and its downstream products, jointly known as jasmonates. As signals, jasmonates have related yet distinct roles in the regulation of plant resistance against insect and pathogen attack. An additional and conceptually parallel pathway involving 9-LOX activity on linoleic acid leads to the production of 10-oxo-11-phytoenoic acid (10-OPEA). Despite structural similarity to jasmonates, physiological roles for 10-OPEA have remained unclear. Both 12-OPDA and 10-OPEA equally promote the transcription of numerous defense genes encoding glutathione S-transferases, cytochrome P450s, and pathogenesis-related proteins; however, 10-OPEA activity diverges in the context of reduced protease inhibitor transcript accumulation. To identify additional differential responses, we subsequently performed whole transcriptome analyses using RNAseq. These comparisons provide a platform for further examination of plant response specificity to the cyclopentenone 10-OPEA. A total of 12 samples were analyzed, comprised of two treatments (10-OPEA and 12-OPDA) and a DMSO carrier control (5%DMSO/0.1%Tween 20 in H20), all in replicates of four.

2015-08-13 | E-GEOD-68589 | biostudies-arrayexpress

OsJAR1M-bM-^HM-^Rrelated JA-inducible genes in osjar1 tos17 mutant rice leaves.

Project description:Jasmonates is inductively produced as a major plant hormone responsible for defense reactions in plants against both biotic and abiotic stresses, such as pathogen infection and mechanical wounding. Jasmonoyl isoleucine is known to be a bioactive compound of jasmonate and plays a pivotal role for plant defenses. We identified OsJAR1M-bM-^HM-^Rrelated JA-inducible genes in osjar1 tos17 mutant (osjar1-2) rice leaves 0 - 2 h after JA treatment using 44k microarray. Expression profiling in the wild-type rice leaves treated with jasmonic acid for 0, 0.5, 1, and 2 h was compared with that in the osjar1 mutant leaves treated with jasmonic acid for 0, 0.5, 1, and 2 h using two-color method with three biological replicates.

2013-03-29 | E-GEOD-45572 | biostudies-arrayexpress

Functional conservation of jasmonate-related MYC transcription factors in Marchantia polymorpha

Project description:The lipid-derived phytohormone jasmonoyl-isoleucine (JA-Ile) regulates plant immunity, growth and development in vascular plants by activating genome-wide transcriptional reprogramming. In Arabidopsis, this is largely orchestrated by the master regulator MYC2 and related transcription factors (TFs). However, the TFs activating this pathway in basal plant lineages are currently unknown. We report the functional conservation of MYC-related TFs between the eudicot Arabidopsis thaliana and the liverwort Marchantia polymorpha, a plant belonging to one of the most basal land-plants lineages. Phylogenetic analysis suggests that MYC function first appeared in charophycean algae, and therefore predates the evolutionary appearance of any other jasmonate pathway component. Marchantia possesses two functionally interchangeable MYC genes, one in females and one in males. Similar to AtMYC2, MpMYCs showed nuclear localization, interaction with JAZ-repressors, and regulation by light. Phenotypic and molecular characterization of loss- or gain-of-function mutants demonstrated that MpMYCs are necessary and sufficient for the activation of the pathway in Marchantia, but unlike their Arabidopsis orthologs, do not regulate fertility. Our results show that despite 450 million years of independent evolution, MYCs are functionally conserved between bryophytes and eudicots. Genetic conservation in one of the most basal lineages suggests that MYC function existed in the common ancestor of land plants and evolved from a pre-existing MYC function in charophycean algae.

2019-03-19 | GSE124159 | GEO

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