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Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha
In plants, jasmonate signaling regulates a wide range of processes from growth and development to defense responses and thermotolerance. Jasmonates, such as jasmonic acid (JA), (+)-7-iso-jasmonoyl-l-isoleucine (JA-Ile), 12-oxo-10,15(Z)-phytodienoic acid (OPDA), and dinor-12-oxo-10,15(Z)-phytodienoic...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9457472/ https://www.ncbi.nlm.nih.gov/pubmed/36037336 http://dx.doi.org/10.1073/pnas.2202930119 |
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author | Kneeshaw, Sophie Soriano, Gonzalo Monte, Isabel Hamberg, Mats Zamarreño, Ángel M. García-Mina, Jose M. Franco-Zorrilla, José Manuel Kato, Nobuki Ueda, Minoru Rey-Stolle, Ma Fernanda Barbas, Coral Michavila, Santiago Gimenez-Ibanez, Selena Jimenez-Aleman, Guillermo H. Solano, Roberto |
author_facet | Kneeshaw, Sophie Soriano, Gonzalo Monte, Isabel Hamberg, Mats Zamarreño, Ángel M. García-Mina, Jose M. Franco-Zorrilla, José Manuel Kato, Nobuki Ueda, Minoru Rey-Stolle, Ma Fernanda Barbas, Coral Michavila, Santiago Gimenez-Ibanez, Selena Jimenez-Aleman, Guillermo H. Solano, Roberto |
author_sort | Kneeshaw, Sophie |
collection | PubMed |
description | In plants, jasmonate signaling regulates a wide range of processes from growth and development to defense responses and thermotolerance. Jasmonates, such as jasmonic acid (JA), (+)-7-iso-jasmonoyl-l-isoleucine (JA-Ile), 12-oxo-10,15(Z)-phytodienoic acid (OPDA), and dinor-12-oxo-10,15(Z)-phytodienoic acid (dn-OPDA), are derived from C18 (18 Carbon atoms) and C16 polyunsaturated fatty acids (PUFAs), which are found ubiquitously in the plant kingdom. Bryophytes are also rich in C20 and C22 long-chain polyunsaturated fatty acids (LCPUFAs), which are found only at low levels in some vascular plants but are abundant in organisms of other kingdoms, including animals. The existence of bioactive jasmonates derived from LCPUFAs is currently unknown. Here, we describe the identification of an OPDA-like molecule derived from a C20 fatty acid (FA) in the liverwort Marchantia polymorpha (Mp), which we term (5Z,8Z)-10-(4-oxo-5-((Z)-pent-2-en-1-yl)cyclopent-2-en-1-yl)deca-5,8-dienoic acid (C20-OPDA). This molecule accumulates upon wounding and, when applied exogenously, can activate known Coronatine Insensitive 1 (COI1) –dependent and –independent jasmonate responses. Furthermore, we identify a dn-OPDA–like molecule (Δ(4)-dn-OPDA) deriving from C20-OPDA and demonstrate it to be a ligand of the jasmonate coreceptor (MpCOI1–Mp Jasmonate-Zinc finger inflorescence meristem domain [MpJAZ]) in Marchantia. By analyzing mutants impaired in the production of LCPUFAs, we elucidate the major biosynthetic pathway of C20-OPDA and Δ(4)-dn-OPDA. Moreover, using a double mutant compromised in the production of both Δ(4)-dn-OPDA and dn-OPDA, we demonstrate the additive nature of these molecules in the activation of jasmonate responses. Taken together, our data identify a ligand of MpCOI1 and demonstrate LCPUFAs as a source of bioactive jasmonates that are essential to the immune response of M. polymorpha. |
format | Online Article Text |
id | pubmed-9457472 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-94574722023-03-01 Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha Kneeshaw, Sophie Soriano, Gonzalo Monte, Isabel Hamberg, Mats Zamarreño, Ángel M. García-Mina, Jose M. Franco-Zorrilla, José Manuel Kato, Nobuki Ueda, Minoru Rey-Stolle, Ma Fernanda Barbas, Coral Michavila, Santiago Gimenez-Ibanez, Selena Jimenez-Aleman, Guillermo H. Solano, Roberto Proc Natl Acad Sci U S A Biological Sciences In plants, jasmonate signaling regulates a wide range of processes from growth and development to defense responses and thermotolerance. Jasmonates, such as jasmonic acid (JA), (+)-7-iso-jasmonoyl-l-isoleucine (JA-Ile), 12-oxo-10,15(Z)-phytodienoic acid (OPDA), and dinor-12-oxo-10,15(Z)-phytodienoic acid (dn-OPDA), are derived from C18 (18 Carbon atoms) and C16 polyunsaturated fatty acids (PUFAs), which are found ubiquitously in the plant kingdom. Bryophytes are also rich in C20 and C22 long-chain polyunsaturated fatty acids (LCPUFAs), which are found only at low levels in some vascular plants but are abundant in organisms of other kingdoms, including animals. The existence of bioactive jasmonates derived from LCPUFAs is currently unknown. Here, we describe the identification of an OPDA-like molecule derived from a C20 fatty acid (FA) in the liverwort Marchantia polymorpha (Mp), which we term (5Z,8Z)-10-(4-oxo-5-((Z)-pent-2-en-1-yl)cyclopent-2-en-1-yl)deca-5,8-dienoic acid (C20-OPDA). This molecule accumulates upon wounding and, when applied exogenously, can activate known Coronatine Insensitive 1 (COI1) –dependent and –independent jasmonate responses. Furthermore, we identify a dn-OPDA–like molecule (Δ(4)-dn-OPDA) deriving from C20-OPDA and demonstrate it to be a ligand of the jasmonate coreceptor (MpCOI1–Mp Jasmonate-Zinc finger inflorescence meristem domain [MpJAZ]) in Marchantia. By analyzing mutants impaired in the production of LCPUFAs, we elucidate the major biosynthetic pathway of C20-OPDA and Δ(4)-dn-OPDA. Moreover, using a double mutant compromised in the production of both Δ(4)-dn-OPDA and dn-OPDA, we demonstrate the additive nature of these molecules in the activation of jasmonate responses. Taken together, our data identify a ligand of MpCOI1 and demonstrate LCPUFAs as a source of bioactive jasmonates that are essential to the immune response of M. polymorpha. National Academy of Sciences 2022-08-29 2022-09-06 /pmc/articles/PMC9457472/ /pubmed/36037336 http://dx.doi.org/10.1073/pnas.2202930119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Kneeshaw, Sophie Soriano, Gonzalo Monte, Isabel Hamberg, Mats Zamarreño, Ángel M. García-Mina, Jose M. Franco-Zorrilla, José Manuel Kato, Nobuki Ueda, Minoru Rey-Stolle, Ma Fernanda Barbas, Coral Michavila, Santiago Gimenez-Ibanez, Selena Jimenez-Aleman, Guillermo H. Solano, Roberto Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title | Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title_full | Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title_fullStr | Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title_full_unstemmed | Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title_short | Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha |
title_sort | ligand diversity contributes to the full activation of the jasmonate pathway in marchantia polymorpha |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9457472/ https://www.ncbi.nlm.nih.gov/pubmed/36037336 http://dx.doi.org/10.1073/pnas.2202930119 |
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