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Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth

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...

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Autores principales: Gasperini, Debora, Chételat, Aurore, Acosta, Ivan F., Goossens, Jonas, Pauwels, Laurens, Goossens, Alain, Dreos, René, Alfonso, Esteban, Farmer, Edward E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4466561/
https://www.ncbi.nlm.nih.gov/pubmed/26070206
http://dx.doi.org/10.1371/journal.pgen.1005300
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author Gasperini, Debora
Chételat, Aurore
Acosta, Ivan F.
Goossens, Jonas
Pauwels, Laurens
Goossens, Alain
Dreos, René
Alfonso, Esteban
Farmer, Edward E.
author_facet Gasperini, Debora
Chételat, Aurore
Acosta, Ivan F.
Goossens, Jonas
Pauwels, Laurens
Goossens, Alain
Dreos, René
Alfonso, Esteban
Farmer, Edward E.
author_sort Gasperini, Debora
collection PubMed
description 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.
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spelling pubmed-44665612015-06-22 Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth Gasperini, Debora Chételat, Aurore Acosta, Ivan F. Goossens, Jonas Pauwels, Laurens Goossens, Alain Dreos, René Alfonso, Esteban Farmer, Edward E. PLoS Genet Research Article 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. Public Library of Science 2015-06-12 /pmc/articles/PMC4466561/ /pubmed/26070206 http://dx.doi.org/10.1371/journal.pgen.1005300 Text en © 2015 Gasperini et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Gasperini, Debora
Chételat, Aurore
Acosta, Ivan F.
Goossens, Jonas
Pauwels, Laurens
Goossens, Alain
Dreos, René
Alfonso, Esteban
Farmer, Edward E.
Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title_full Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title_fullStr Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title_full_unstemmed Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title_short Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth
title_sort multilayered organization of jasmonate signalling in the regulation of root growth
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4466561/
https://www.ncbi.nlm.nih.gov/pubmed/26070206
http://dx.doi.org/10.1371/journal.pgen.1005300
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