Suppression of Plant Immunity by Fungal Chitinase-like Effectors

Crop diseases caused by fungi constitute one of the most important problems in agriculture, posing a serious threat to food security [1]. To establish infection, phytopathogens interfere with plant immune responses [2, 3]. However, strategies to promote virulence employed by fungal pathogens, especi...

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Detalhes bibliográficos
Autores: Fiorin, Gabriel Lorencini, Sánchez-Vallet, Andrea, Toledo Thomazella, Daniela Paula de, Vital do Prado, Paula Favoretti, Costa do Nascimento, Leandro, Oliveira Figueira, Antonio Vargas de, Thomma, Bart P. H. J., Amarante Guimarães Pereira, Gonçalo, Pereira Lima Teixeira, Paulo José
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2018
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/415468
Acesso em linha:http://hdl.handle.net/10261/415468
https://api.elsevier.com/content/abstract/scopus_id/85056486934
Access Level:acceso abierto
Palavra-chave:Witches’ broom disease
GH18
LysM
MAMP-triggered immunity
Moniliophthora
Cacao
Chitin
Effector
Frosty pod rot
Neofunctionalization
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spelling Suppression of Plant Immunity by Fungal Chitinase-like EffectorsFiorin, Gabriel LorenciniSánchez-Vallet, AndreaToledo Thomazella, Daniela Paula deVital do Prado, Paula FavorettiCosta do Nascimento, LeandroOliveira Figueira, Antonio Vargas deThomma, Bart P. H. J.Amarante Guimarães Pereira, GonçaloPereira Lima Teixeira, Paulo JoséWitches’ broom diseaseGH18LysMMAMP-triggered immunityMoniliophthoraCacaoChitinEffectorFrosty pod rotNeofunctionalizationCrop diseases caused by fungi constitute one of the most important problems in agriculture, posing a serious threat to food security [1]. To establish infection, phytopathogens interfere with plant immune responses [2, 3]. However, strategies to promote virulence employed by fungal pathogens, especially non-model organisms, remain elusive [4], mainly because fungi are more complex and difficult to study when compared to the better-characterized bacterial pathogens. Equally incomplete is our understanding of the birth of microbial virulence effectors. Here, we show that the cacao pathogen Moniliophthora perniciosa evolved an enzymatically inactive chitinase (MpChi) that functions as a putative pathogenicity factor. MpChi is among the most highly expressed fungal genes during the biotrophic interaction with cacao and encodes a chitinase with mutations that abolish its enzymatic activity. Despite the lack of chitinolytic activity, MpChi retains substrate binding specificity and prevents chitin-triggered immunity by sequestering immunogenic chitin fragments. Remarkably, its sister species M. roreri encodes a second non-orthologous catalytically impaired chitinase with equivalent function. Thus, a class of conserved enzymes independently evolved as putative virulence factors in these fungi. In addition to unveiling a strategy of host immune suppression by fungal pathogens, our results demonstrate that the neofunctionalization of enzymes may be an evolutionary pathway for the rise of new virulence factors in fungi. We anticipate that analogous strategies are likely employed by other pathogens.This research was supported by the São Paulo Research Foundation (FAPESP) through fellowships to G.L.F. (11/23315-1, 13/09878-9, and 14/06181-0) and P.J.P.L.T. (09/51018-1) and grants to G.A.G.P. (09/50119-9 and 16/10498-4).Peer reviewedElsevierCell PressSao Paulo Research FoundationSánchez-Vallet, Andrea [0000-0002-3668-9503]202620262018info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/415468https://api.elsevier.com/content/abstract/scopus_id/85056486934reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.cub.2018.07.055https://doi.org/10.1016/j.cub.2018.07.055Noinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4154682026-05-22T06:33:51Z
dc.title.none.fl_str_mv Suppression of Plant Immunity by Fungal Chitinase-like Effectors
title Suppression of Plant Immunity by Fungal Chitinase-like Effectors
spellingShingle Suppression of Plant Immunity by Fungal Chitinase-like Effectors
Fiorin, Gabriel Lorencini
Witches’ broom disease
GH18
LysM
MAMP-triggered immunity
Moniliophthora
Cacao
Chitin
Effector
Frosty pod rot
Neofunctionalization
title_short Suppression of Plant Immunity by Fungal Chitinase-like Effectors
title_full Suppression of Plant Immunity by Fungal Chitinase-like Effectors
title_fullStr Suppression of Plant Immunity by Fungal Chitinase-like Effectors
title_full_unstemmed Suppression of Plant Immunity by Fungal Chitinase-like Effectors
title_sort Suppression of Plant Immunity by Fungal Chitinase-like Effectors
dc.creator.none.fl_str_mv Fiorin, Gabriel Lorencini
Sánchez-Vallet, Andrea
Toledo Thomazella, Daniela Paula de
Vital do Prado, Paula Favoretti
Costa do Nascimento, Leandro
Oliveira Figueira, Antonio Vargas de
Thomma, Bart P. H. J.
Amarante Guimarães Pereira, Gonçalo
Pereira Lima Teixeira, Paulo José
author Fiorin, Gabriel Lorencini
author_facet Fiorin, Gabriel Lorencini
Sánchez-Vallet, Andrea
Toledo Thomazella, Daniela Paula de
Vital do Prado, Paula Favoretti
Costa do Nascimento, Leandro
Oliveira Figueira, Antonio Vargas de
Thomma, Bart P. H. J.
Amarante Guimarães Pereira, Gonçalo
Pereira Lima Teixeira, Paulo José
author_role author
author2 Sánchez-Vallet, Andrea
Toledo Thomazella, Daniela Paula de
Vital do Prado, Paula Favoretti
Costa do Nascimento, Leandro
Oliveira Figueira, Antonio Vargas de
Thomma, Bart P. H. J.
Amarante Guimarães Pereira, Gonçalo
Pereira Lima Teixeira, Paulo José
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Sao Paulo Research Foundation
Sánchez-Vallet, Andrea [0000-0002-3668-9503]
dc.subject.none.fl_str_mv Witches’ broom disease
GH18
LysM
MAMP-triggered immunity
Moniliophthora
Cacao
Chitin
Effector
Frosty pod rot
Neofunctionalization
topic Witches’ broom disease
GH18
LysM
MAMP-triggered immunity
Moniliophthora
Cacao
Chitin
Effector
Frosty pod rot
Neofunctionalization
description Crop diseases caused by fungi constitute one of the most important problems in agriculture, posing a serious threat to food security [1]. To establish infection, phytopathogens interfere with plant immune responses [2, 3]. However, strategies to promote virulence employed by fungal pathogens, especially non-model organisms, remain elusive [4], mainly because fungi are more complex and difficult to study when compared to the better-characterized bacterial pathogens. Equally incomplete is our understanding of the birth of microbial virulence effectors. Here, we show that the cacao pathogen Moniliophthora perniciosa evolved an enzymatically inactive chitinase (MpChi) that functions as a putative pathogenicity factor. MpChi is among the most highly expressed fungal genes during the biotrophic interaction with cacao and encodes a chitinase with mutations that abolish its enzymatic activity. Despite the lack of chitinolytic activity, MpChi retains substrate binding specificity and prevents chitin-triggered immunity by sequestering immunogenic chitin fragments. Remarkably, its sister species M. roreri encodes a second non-orthologous catalytically impaired chitinase with equivalent function. Thus, a class of conserved enzymes independently evolved as putative virulence factors in these fungi. In addition to unveiling a strategy of host immune suppression by fungal pathogens, our results demonstrate that the neofunctionalization of enzymes may be an evolutionary pathway for the rise of new virulence factors in fungi. We anticipate that analogous strategies are likely employed by other pathogens.
publishDate 2018
dc.date.none.fl_str_mv 2018
2026
2026
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/10261/415468
https://api.elsevier.com/content/abstract/scopus_id/85056486934
url http://hdl.handle.net/10261/415468
https://api.elsevier.com/content/abstract/scopus_id/85056486934
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.cub.2018.07.055
https://doi.org/10.1016/j.cub.2018.07.055
No
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 Elsevier
Cell Press
publisher.none.fl_str_mv Elsevier
Cell Press
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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