title: Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth.
abstract: Physical damage can strongly affect plant growth, reducing the biomass of developing organs situated at a distance from wounds. These effects, previously studied in leaves, require the activation of jasmonate (JA) signalling. Using a novel assay involving repetitive cotyledon wounding in Arabidopsis seedlings, we uncovered a function of JA in suppressing cell division and elongation in roots. Regulatory JA signalling components were then manipulated to delineate their relative impacts on root growth. The new transcription factor mutant myc2-322B was isolated. In vitro transcription assays and whole-plant approaches revealed that myc2-322B is a dosage-dependent gain-of-function mutant that can amplify JA growth responses. Moreover, myc2-322B displayed extreme hypersensitivity to JA that totally suppressed root elongation. The mutation weakly reduced root growth in undamaged plants but, when the upstream negative regulator NINJA was genetically removed, myc2-322B powerfully repressed root growth through its effects on cell division and cell elongation. Furthermore, in a JA-deficient mutant background, ninja1 myc2-322B still repressed root elongation, indicating that it is possible to generate JA-responses in the absence of JA. We show that NINJA forms a broadly expressed regulatory layer that is required to inhibit JA signalling in the apex of roots grown under basal conditions. By contrast, MYC2, MYC3 and MYC4 displayed cell layer-specific localisations and MYC3 and MYC4 were expressed in mutually exclusive regions. In nature, growing roots are likely subjected to constant mechanical stress during soil penetration that could lead to JA production and subsequent detrimental effects on growth. Our data reveal how distinct negative regulatory layers, including both NINJA-dependent and -independent mechanisms, restrain JA responses to allow normal root growth. Mechanistic insights from this work underline the importance of mapping JA signalling components to specific cell types in order to understand and potentially engineer the growth reduction that follows physical damage.
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.
authors.forename: Debora
authors.initials: D
authors.lastname: Gasperini
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.
authors.forename: Aurore
authors.initials: A
authors.lastname: Chételat
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.
authors.forename: Ivan F
authors.initials: IF
authors.lastname: Acosta
authors.affiliation: Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium.
authors.forename: Jonas
authors.initials: J
authors.lastname: Goossens
authors.affiliation: Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium.
authors.forename: Laurens
authors.initials: L
authors.lastname: Pauwels
authors.affiliation: Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium.
authors.forename: Alain
authors.initials: A
authors.lastname: Goossens
authors.affiliation: Swiss Institute of Bioinformatics, Lausanne, Switzerland.
authors.forename: René
authors.initials: R
authors.lastname: Dreos
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.
authors.forename: Esteban
authors.initials: E
authors.lastname: Alfonso
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.
authors.forename: Edward E
authors.initials: EE
authors.lastname: Farmer
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D051778:Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / Q000235:genetics / Q000378:metabolism; D003517:Cyclopentanes / Q000494:pharmacology*; D054883:Oxylipins / Q000494:pharmacology*; D018517:Plant Roots / Q000187:drug effects / Q000254:growth & development* / Q000378:metabolism; D015290:Second Messenger Systems
chemical_list: D029681:Arabidopsis Proteins; D051778:Basic Helix-Loop-Helix Leucine Zipper Transcription Factors; D003517:Cyclopentanes; C473611:MYC2 protein, Arabidopsis; D054883:Oxylipins; C011006:jasmonic acid