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Rational design of a ligand-based antagonist of jasmonate perception

ABSTRACT: 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.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE56027 | GEO | 2014/06/20

SECONDARY ACCESSION(S): PRJNA242256

REPOSITORIES: GEO

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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. Two-condition experiment, Col-0 vs Col-0 plants treated 2h with Coronatine 0-methyloxime (COR-MO) and Col-0 plants treated 2h with Coronatine vs Col-0 plants treated 2h with Coronatine plus COR-MO. Biological replicates: 4 control and 4 treated replicates

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

Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection

Project description:Pathogens target phytohormone signalling pathways to promote disease. Plants deploy salicylic acid (SA) mediated defences against biotrophs. Pathogens antagonise SA immunity by activating jasmonate signalling, e.g. Pseudomonas syringae pv. tomato DC3000 produces coronatine (COR), a jasmonate (JA) mimic. This study found unexpected dynamics between SA, JA and COR and co-operation between JAZ jasmonate repressor proteins during DC3000 infection. JA did not accumulate until late in the infection process and was higher in leaves challenged with coronatine deficient P. syringae or in the more resistant JA receptor mutant coi1. JAZ regulation was complex and coronatine alone was insufficient to sustainably induce JAZs.

2015-08-28 | GSE72461 | GEO

Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection

2015-08-28 | E-GEOD-72461 | biostudies-arrayexpress

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

Fine kinetic transcriptome analysis during jasmonate signaling

Project description:To study the role of the plant hormone jasmonate in regulating stress-induced allocation of photosynthetic products between growth- and defense-related processes, we used RNA-sequencing to query the Arabidopsis transcriptome at high temporal resolution over 24 h after treatment with the bacterial toxin coronatine (COR, 5 micromolar), a high-affinity agonist of the JA receptor, or with a mock solution to account for diurnal changes in gene expression. These data establish a fine-scale view of the kinetics of jasmonate signaling, as well as of the diurnal patterns of gene expression.

2015-06-01 | E-MTAB-4218 | biostudies-arrayexpress

Arabidopsis ECAP is a New Adaptor Protein that Connects JAZ Repressors with TPR2 Co-repressor to Suppress Jasmonate-Responsive Anthocyanin Accumulation

Project description:Suppression mechanism employed by transcriptional repressors is commonly existed in diverse phytohormone signaling. In Arabidopsis thaliana, JASMONATE-ZIM DOMAIN (JAZ) proteins act as transcriptional repressors and involve in different aspects of the JA signaling network, through recruiting general co-repressors TOPLESS (TPL) and TPL-related proteins (TPRs). To accomplish overlapping but also finely separated functions of JAZ proteins, specificadaptor proteins are employed in JA signaling. Novel Interactor of JAZ (NINJA) is an adaptor protein mediates gene repression in JA-dependent root growth inhibition and pathogen defense. However, the adaptor protein(s) modulate other JA responsive biological processes is still a mystery. In this study, we demonstrated that a previously uncharacterized protein, ECAP(EAR-Containing Adaptor Protein) that connects JAZ6/8 and TPR to repress JA-mediated anthocyanin accumulation at low JA level. We also found ECAP-mediated transcriptional repression might play a general role in multiple aspects of plant development and responses to environments.

2019-11-07 | GSE125557 | GEO

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

Project description: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.

2022-01-11 | GSE186451 | GEO

CONSTANS and jasmonate signaling coordinate floral senescence in Arabidopsis

Project description:Photoperiodic floral initiation in the leaf is controlled by the hub gene CONSTANS (CO) while jasmonates (JAs) control flower senescence. Although both processes are chronologically ordered, no association between them has been described to date. We show that CO protein remains in Arabidopsis flowers after the floral induction, although displaying a different tissue and diurnal pattern than in leaves. We found that changes in CO expression alter flower senescence and abscission by interfering with the JA response, supported by petal specific analysis as well as CO overexpression in JA synthesis and signaling mutants. CO has a ZIM-like domain that mediates interaction with the JA response repressor JAZ3 (jasmonate ZIM-domain 3), inhibiting its repressor activity and activating downstream transcription factors involved in flower senescence. The complex CO-JAZ3 also interacts with the E3 ubiquitin ligase Coronatine Insensitive 1 (COI1) leading to its degradation in the presence of jasmonates. Therefore, the coordinated recruitment of photoperiodic and jasmonate signaling pathways would be an efficient way for plants to chronologically order the floral process and ensure the success of offspring production.

2022-09-26 | GSE204774 | GEO

An Ancient COI1-independent Function for Reactive Electrophilic Oxylipins in Thermotolerance [array]

Project description:Seeds of the double mutant opr3-3 coi1-1 were germinated in Johnson media supplemented with 0.5 µM coronatine, to select homozygous coi1-1 plants, at 21°C under long-day conditions (16-h light/8-h dark)

2020-03-04 | GSE141429 | GEO

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