The tomato P69 subtilase family is involved in resistance to bacterial wilt

The intercellular space or apoplast constitutes the main interface in plant-pathogen interactions. Apoplastic subtilisin-like proteases-subtilases-may play an important role in defence and they have been identified as targets of pathogen-secreted effector proteins. Here, we characterise the role of...

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Authors: Zhang, Weiqi, Planas-Marquès, Marc, Mazier, Marianne, Šimkovicová, Margarita, Rocafort, Mercedes, Mantz, Melissa, Huesgen, Pitter F, Takken, Frank L. W., Stintzi, Annick, Schaller, Andreas, Coll, Núria S., Valls, Marc
Format: article
Status:Published version
Publication Date:2024
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/372572
Online Access:http://hdl.handle.net/10261/372572
https://api.elsevier.com/content/abstract/scopus_id/85180897855
Access Level:Open access
Keyword:Apoplast
Plant defence
Ralstonia solanacearum
Serine protease
Solanum lycopersicum
id ES_87c05c94801210a692fbdfd721cf7d33
oai_identifier_str oai:digital.csic.es:10261/372572
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv The tomato P69 subtilase family is involved in resistance to bacterial wilt
title The tomato P69 subtilase family is involved in resistance to bacterial wilt
spellingShingle The tomato P69 subtilase family is involved in resistance to bacterial wilt
Zhang, Weiqi
Apoplast
Plant defence
Ralstonia solanacearum
Serine protease
Solanum lycopersicum
title_short The tomato P69 subtilase family is involved in resistance to bacterial wilt
title_full The tomato P69 subtilase family is involved in resistance to bacterial wilt
title_fullStr The tomato P69 subtilase family is involved in resistance to bacterial wilt
title_full_unstemmed The tomato P69 subtilase family is involved in resistance to bacterial wilt
title_sort The tomato P69 subtilase family is involved in resistance to bacterial wilt
dc.creator.none.fl_str_mv Zhang, Weiqi
Planas-Marquès, Marc
Mazier, Marianne
Šimkovicová, Margarita
Rocafort, Mercedes
Mantz, Melissa
Huesgen, Pitter F
Takken, Frank L. W.
Stintzi, Annick
Schaller, Andreas
Coll, Núria S.
Valls, Marc
author Zhang, Weiqi
author_facet Zhang, Weiqi
Planas-Marquès, Marc
Mazier, Marianne
Šimkovicová, Margarita
Rocafort, Mercedes
Mantz, Melissa
Huesgen, Pitter F
Takken, Frank L. W.
Stintzi, Annick
Schaller, Andreas
Coll, Núria S.
Valls, Marc
author_role author
author2 Planas-Marquès, Marc
Mazier, Marianne
Šimkovicová, Margarita
Rocafort, Mercedes
Mantz, Melissa
Huesgen, Pitter F
Takken, Frank L. W.
Stintzi, Annick
Schaller, Andreas
Coll, Núria S.
Valls, Marc
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
European Commission
Generalitat de Catalunya
Agence Nationale de la Recherche (France)
Takken, Frank L. W. [0000-0003-2655-3108]
Coll, Núria S. [0000-0002-8889-0399]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Apoplast
Plant defence
Ralstonia solanacearum
Serine protease
Solanum lycopersicum
topic Apoplast
Plant defence
Ralstonia solanacearum
Serine protease
Solanum lycopersicum
description The intercellular space or apoplast constitutes the main interface in plant-pathogen interactions. Apoplastic subtilisin-like proteases-subtilases-may play an important role in defence and they have been identified as targets of pathogen-secreted effector proteins. Here, we characterise the role of the Solanaceae-specific P69 subtilase family in the interaction between tomato and the vascular bacterial wilt pathogen Ralstonia solanacearum. R. solanacearum infection post-translationally activated several tomato P69s. Among them, P69D was exclusively activated in tomato plants resistant to R. solanacearum. In vitro experiments showed that P69D activation by prodomain removal occurred in an autocatalytic and intramolecular reaction that does not rely on the residue upstream of the processing site. Importantly P69D-deficient tomato plants were more susceptible to bacterial wilt and transient expression of P69B, D and G in Nicotiana benthamiana limited proliferation of R. solanacearum. Our study demonstrates that P69s have conserved features but diverse functions in tomato and that P69D is involved in resistance to R. solanacearum but not to other vascular pathogens like Fusarium oxysporum.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
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/10261/372572
https://api.elsevier.com/content/abstract/scopus_id/85180897855
url http://hdl.handle.net/10261/372572
https://api.elsevier.com/content/abstract/scopus_id/85180897855
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-108595RB-I00
info:eu-repo/grantAgreement/AEI//TED2021-131457B-I00
info:eu-repo/grantAgreement/AEI//CEX2019-000917
The Plant journal : for cell and molecular biology
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://dx.doi.org/10.1111/tpj.16613
Huesgen, Pitter; 2024; Comparison of tomato wild type and P69D knock-out mutant apoplast proteome and N-terminomes [Dataset]; Proteome Xchange; PXD044635
Huesgen, Pitter; 2024; N-terminome analysis of tomato P69D knock-out mutant total leaf proteomes treated with and without recominant P69D [Dataset]; Proteome Xchange; PXD044637
http://dx.doi.org/10.1111/tpj.16613
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
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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spelling The tomato P69 subtilase family is involved in resistance to bacterial wiltZhang, WeiqiPlanas-Marquès, MarcMazier, MarianneŠimkovicová, MargaritaRocafort, MercedesMantz, MelissaHuesgen, Pitter FTakken, Frank L. W.Stintzi, AnnickSchaller, AndreasColl, Núria S.Valls, MarcApoplastPlant defenceRalstonia solanacearumSerine proteaseSolanum lycopersicumThe intercellular space or apoplast constitutes the main interface in plant-pathogen interactions. Apoplastic subtilisin-like proteases-subtilases-may play an important role in defence and they have been identified as targets of pathogen-secreted effector proteins. Here, we characterise the role of the Solanaceae-specific P69 subtilase family in the interaction between tomato and the vascular bacterial wilt pathogen Ralstonia solanacearum. R. solanacearum infection post-translationally activated several tomato P69s. Among them, P69D was exclusively activated in tomato plants resistant to R. solanacearum. In vitro experiments showed that P69D activation by prodomain removal occurred in an autocatalytic and intramolecular reaction that does not rely on the residue upstream of the processing site. Importantly P69D-deficient tomato plants were more susceptible to bacterial wilt and transient expression of P69B, D and G in Nicotiana benthamiana limited proliferation of R. solanacearum. Our study demonstrates that P69s have conserved features but diverse functions in tomato and that P69D is involved in resistance to R. solanacearum but not to other vascular pathogens like Fusarium oxysporum.Research was funded by grant MCIN/AEI/PID2019-108595RB-I00 funded by MCIN/AEI/10.13039/501100011033 (to N.S.C. and M.V.), grant TED2021-131457B-I00 funded by MCIN/AEI/10.13039/501100011033 and by the ‘European Union NextGenerationEU/PRTR’ (to N.S.C. and M.V.), through the ‘Severo Ochoa Programme for Centres of Excellence in R&D’ (CEX2019-000917 funded by MCIN/AEI/10.13039/501100011033), and by the CERCA Program of the Catalan government (Generalitat de Catalunya). M.S. and F.L.W.T. obtained support from the NWO-Earth and Life Sciences funded VICI Project No. 865.14.003. W.Z. was the recipient of a CSC Fellowship CSC201906990041. M.P.-M. was the recipient of an FPU grant (FPU15/02125) funded by Ministerio de Universidades. GAFL UR1052 benefits from the support of the French National Agency (ANR11-BTBR-0001-GENIUS). We acknowledge the support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).With funding from the Spanish goverment through the "Severo Ochoa Centre of Excellence" accreditation (CEX2019-000917)Peer reviewedJohn Wiley & SonsMinisterio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)European CommissionGeneralitat de CatalunyaAgence Nationale de la Recherche (France)Takken, Frank L. W. [0000-0003-2655-3108]Coll, Núria S. [0000-0002-8889-0399]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/372572https://api.elsevier.com/content/abstract/scopus_id/85180897855reponame: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/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-108595RB-I00info:eu-repo/grantAgreement/AEI//TED2021-131457B-I00info:eu-repo/grantAgreement/AEI//CEX2019-000917The Plant journal : for cell and molecular biologyThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://dx.doi.org/10.1111/tpj.16613Huesgen, Pitter; 2024; Comparison of tomato wild type and P69D knock-out mutant apoplast proteome and N-terminomes [Dataset]; Proteome Xchange; PXD044635Huesgen, Pitter; 2024; N-terminome analysis of tomato P69D knock-out mutant total leaf proteomes treated with and without recominant P69D [Dataset]; Proteome Xchange; PXD044637http://dx.doi.org/10.1111/tpj.16613Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3725722026-05-22T06:33:51Z
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