Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism

Plants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.1 Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subseq...

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Autores: Marquès-Bueno, Maria Mar, Armengot, Laia, Noack, Lise C., Bareille, Joseph, Rodríguez, Lesia, Pierre Platre, Matthieu, Bayle, Vincent, Liu, Mengying, Opdenacker, Davy, Vanneste, Steffen, Möller, Barbara K., Nimchuk, Zachary L., Beeckman, Tom, Caño-Delgado, Ana I., Friml, Jiří, Jaillais, Yvon
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/253760
Acceso en línea:http://hdl.handle.net/10261/253760
Access Level:acceso abierto
Palabra clave:Auxin
Anionic lipids
Brassinosteroid
Gravitropism
Receptor-like kinase
Root
ROP6
MAKR
TMK
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spelling Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropismMarquès-Bueno, Maria MarArmengot, LaiaNoack, Lise C.Bareille, JosephRodríguez, LesiaPierre Platre, MatthieuBayle, VincentLiu, MengyingOpdenacker, DavyVanneste, SteffenMöller, Barbara K.Nimchuk, Zachary L.Beeckman, TomCaño-Delgado, Ana I.Friml, JiříJaillais, YvonAuxinAnionic lipidsBrassinosteroidGravitropismReceptor-like kinaseRootROP6MAKRTMKPlants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.1 Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subsequent reset of auxin distribution back to the original pre-gravistimulation situation.1, 2, 3 Differential auxin accumulation during the gravitropic response depends on the activity of polarly localized PIN-FORMED (PIN) auxin-efflux carriers.1, 2, 3, 4 In particular, the timing of this dynamic response is regulated by PIN2,5,6 but the underlying molecular mechanisms are poorly understood. Here, we show that MEMBRANE ASSOCIATED KINASE REGULATOR2 (MAKR2) controls the pace of the root gravitropic response. We found that MAKR2 is required for the PIN2 asymmetry during gravitropism by acting as a negative regulator of the cell-surface signaling mediated by the receptor-like kinase TRANSMEMBRANE KINASE1 (TMK1).2,7, 8, 9, 10 Furthermore, we show that the MAKR2 inhibitory effect on TMK1 signaling is antagonized by auxin itself, which triggers rapid MAKR2 membrane dissociation in a TMK1-dependent manner. Our findings suggest that the timing of the root gravitropic response is orchestrated by the reversible inhibition of the TMK1 signaling pathway at the cell surface.Y.J. was funded by ERC grant 3363360-APPL under FP/2007–2013. Y.J. and Z.L.N. were funded by an ANR- and NSF-supported ERA-CAPS project (SICOPID: ANR-17-CAPS-0003-01/NSF PGRP IOS-1841917). A.I.C.-D. is funded by an ERC consolidator grant (ERC-2015-CoG–683163) and BIO2016-78955 grant from the Spanish Ministry of Economy and Competitiveness. Exchanges between the Y.J. and T.B. laboratories were funded by Tournesol grant 35656NB. B.K.M. was funded by the Omics@vib Marie Curie COFUND and Research Foundation Flanders for a postdoctoral fellowship.Peer reviewedElsevierEuropean Research CouncilEuropean CommissionAgence Nationale de la Recherche (France)Ministerio de Economía y Competitividad (España)National Science Foundation (US)Research Foundation - FlandersConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202120212021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/253760reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/FP7/336360info:eu-repo/grantAgreement/EC/H2020/683163info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2016-78955-Phttps://doi.org/10.1016/j.cub.2020.10.011Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2537602026-05-22T06:33:51Z
dc.title.none.fl_str_mv Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
title Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
spellingShingle Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
Marquès-Bueno, Maria Mar
Auxin
Anionic lipids
Brassinosteroid
Gravitropism
Receptor-like kinase
Root
ROP6
MAKR
TMK
title_short Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
title_full Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
title_fullStr Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
title_full_unstemmed Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
title_sort Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism
dc.creator.none.fl_str_mv Marquès-Bueno, Maria Mar
Armengot, Laia
Noack, Lise C.
Bareille, Joseph
Rodríguez, Lesia
Pierre Platre, Matthieu
Bayle, Vincent
Liu, Mengying
Opdenacker, Davy
Vanneste, Steffen
Möller, Barbara K.
Nimchuk, Zachary L.
Beeckman, Tom
Caño-Delgado, Ana I.
Friml, Jiří
Jaillais, Yvon
author Marquès-Bueno, Maria Mar
author_facet Marquès-Bueno, Maria Mar
Armengot, Laia
Noack, Lise C.
Bareille, Joseph
Rodríguez, Lesia
Pierre Platre, Matthieu
Bayle, Vincent
Liu, Mengying
Opdenacker, Davy
Vanneste, Steffen
Möller, Barbara K.
Nimchuk, Zachary L.
Beeckman, Tom
Caño-Delgado, Ana I.
Friml, Jiří
Jaillais, Yvon
author_role author
author2 Armengot, Laia
Noack, Lise C.
Bareille, Joseph
Rodríguez, Lesia
Pierre Platre, Matthieu
Bayle, Vincent
Liu, Mengying
Opdenacker, Davy
Vanneste, Steffen
Möller, Barbara K.
Nimchuk, Zachary L.
Beeckman, Tom
Caño-Delgado, Ana I.
Friml, Jiří
Jaillais, Yvon
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv European Research Council
European Commission
Agence Nationale de la Recherche (France)
Ministerio de Economía y Competitividad (España)
National Science Foundation (US)
Research Foundation - Flanders
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Auxin
Anionic lipids
Brassinosteroid
Gravitropism
Receptor-like kinase
Root
ROP6
MAKR
TMK
topic Auxin
Anionic lipids
Brassinosteroid
Gravitropism
Receptor-like kinase
Root
ROP6
MAKR
TMK
description Plants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.1 Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subsequent reset of auxin distribution back to the original pre-gravistimulation situation.1, 2, 3 Differential auxin accumulation during the gravitropic response depends on the activity of polarly localized PIN-FORMED (PIN) auxin-efflux carriers.1, 2, 3, 4 In particular, the timing of this dynamic response is regulated by PIN2,5,6 but the underlying molecular mechanisms are poorly understood. Here, we show that MEMBRANE ASSOCIATED KINASE REGULATOR2 (MAKR2) controls the pace of the root gravitropic response. We found that MAKR2 is required for the PIN2 asymmetry during gravitropism by acting as a negative regulator of the cell-surface signaling mediated by the receptor-like kinase TRANSMEMBRANE KINASE1 (TMK1).2,7, 8, 9, 10 Furthermore, we show that the MAKR2 inhibitory effect on TMK1 signaling is antagonized by auxin itself, which triggers rapid MAKR2 membrane dissociation in a TMK1-dependent manner. Our findings suggest that the timing of the root gravitropic response is orchestrated by the reversible inhibition of the TMK1 signaling pathway at the cell surface.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/253760
url http://hdl.handle.net/10261/253760
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/FP7/336360
info:eu-repo/grantAgreement/EC/H2020/683163
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2016-78955-P
https://doi.org/10.1016/j.cub.2020.10.011
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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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