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...

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Autores: Kneeshaw, Sophie, Soriano, Gonzalo, Monte, Isabel, Hamberg, Mats, Zamarreño, Ángel M., García-Mina, José M., Franco-Zorrilla, José Manuel, Kato, Nobuki, Ueda, Minoru, Rey-Stolle, Ma Fernanda, Barbas, Coral, Michavila, Santiago, Giménez-Ibáñez, Selena, Jiménez-Alemán, Guillermo H., Solano, Roberto
Tipo de recurso: artículo
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/344379
Acceso en línea:http://hdl.handle.net/10261/344379
https://doi.org/10.1073/pnas.2202930119
Access Level:acceso abierto
Palabra clave:Marchantia
dn-OPDA
jasmonate
phytohormone
plant signaling
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network_name_str España
repository_id_str
spelling Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorphaKneeshaw, SophieSoriano, GonzaloMonte, IsabelHamberg, MatsZamarreño, Ángel M.García-Mina, José M.Franco-Zorrilla, José ManuelKato, NobukiUeda, MinoruRey-Stolle, Ma FernandaBarbas, CoralMichavila, SantiagoGiménez-Ibáñez, SelenaJiménez-Alemán, Guillermo H.Solano, RobertoMarchantiadn-OPDAjasmonatephytohormoneplant signalingIn 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 (Δ4-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 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 a ligand of MpCOI1 and demonstrate LCPUFAs as a source of bioactive jasmonates that are essential to the immune response of M. polymorpha.Peer reviewedNational Academy of Sciences (U.S.)0000-0001-6769-7349Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501http://hdl.handle.net/10261/344379https://doi.org/10.1073/pnas.2202930119reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésProceedings of the National Academy of SciencesSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3443792026-05-22T06:33:51Z
dc.title.none.fl_str_mv 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
spellingShingle Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha
Kneeshaw, Sophie
Marchantia
dn-OPDA
jasmonate
phytohormone
plant signaling
title_short 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_sort Ligand diversity contributes to the full activation of the jasmonate pathway in Marchantia polymorpha
dc.creator.none.fl_str_mv Kneeshaw, Sophie
Soriano, Gonzalo
Monte, Isabel
Hamberg, Mats
Zamarreño, Ángel M.
García-Mina, José M.
Franco-Zorrilla, José Manuel
Kato, Nobuki
Ueda, Minoru
Rey-Stolle, Ma Fernanda
Barbas, Coral
Michavila, Santiago
Giménez-Ibáñez, Selena
Jiménez-Alemán, Guillermo H.
Solano, Roberto
author Kneeshaw, Sophie
author_facet Kneeshaw, Sophie
Soriano, Gonzalo
Monte, Isabel
Hamberg, Mats
Zamarreño, Ángel M.
García-Mina, José M.
Franco-Zorrilla, José Manuel
Kato, Nobuki
Ueda, Minoru
Rey-Stolle, Ma Fernanda
Barbas, Coral
Michavila, Santiago
Giménez-Ibáñez, Selena
Jiménez-Alemán, Guillermo H.
Solano, Roberto
author_role author
author2 Soriano, Gonzalo
Monte, Isabel
Hamberg, Mats
Zamarreño, Ángel M.
García-Mina, José M.
Franco-Zorrilla, José Manuel
Kato, Nobuki
Ueda, Minoru
Rey-Stolle, Ma Fernanda
Barbas, Coral
Michavila, Santiago
Giménez-Ibáñez, Selena
Jiménez-Alemán, Guillermo H.
Solano, Roberto
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv 0000-0001-6769-7349
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Marchantia
dn-OPDA
jasmonate
phytohormone
plant signaling
topic Marchantia
dn-OPDA
jasmonate
phytohormone
plant signaling
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 (Δ4-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 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 a ligand of MpCOI1 and demonstrate LCPUFAs as a source of bioactive jasmonates that are essential to the immune response of M. polymorpha.
publishDate 2022
dc.date.none.fl_str_mv 2022
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/344379
https://doi.org/10.1073/pnas.2202930119
url http://hdl.handle.net/10261/344379
https://doi.org/10.1073/pnas.2202930119
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Proceedings of the National Academy of Sciences
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv National Academy of Sciences (U.S.)
publisher.none.fl_str_mv National Academy of Sciences (U.S.)
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.811543

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