Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity

Autores
Rosli, Hernan Guillermo; Zhen, Yi; Pombo, Marina Alejandra; Zhong, Silin; Bombarely, Aureliano; Fei, Zhangjun; Collmer, Alan; Martin, Gregory B.
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Microbe-associated molecular patterns, such as those present in bacterial flagellin, are powerful inducers of the innate immune response in plants. Successful pathogens deliver virulence proteins, termed effectors, into the plant cell where they can interfere with the immune response and promote disease. Engineering the plant immune system to enhance disease resistance requires a thorough understanding of its components. Results: We describe a high-throughput screen, using RNA sequencing and virus-induced gene silencing, to identify tomato genes whose expression is enhanced by the flagellin microbe-associated molecular pattern flgII-28, but reduced by activities of the Pseudomonas syringae pv. tomato (Pst) type III effectors AvrPto and AvrPtoB. Gene ontology terms for this category of Flagellin-induced repressed by effectors (FIRE) genes showed enrichment for genes encoding certain subfamilies of protein kinases and transcription factors. At least 25 of the FIRE genes have been implicated previously in plant immunity. Of the 92 protein kinase-encoding FIRE genes, 33 were subjected to virus-induced gene silencing and their involvement in pattern-triggered immunity was tested with a leaf-based assay. Silencing of one FIRE gene, which encodes the cell wall-associated kinase SlWAK1, compromised the plant immune response resulting in increased growth of Pst and enhanced disease symptoms. Conclusions: Our transcriptomic approach identifies FIRE genes that represent a pathogen-defined core set of immune-related genes. The analysis of this set of candidate genes led to the discovery of a cell wall-associated kinase that participates in plant defense. The FIRE genes will be useful for further elucidation of the plant immune system.
Fil: Rosli, Hernan Guillermo. Boyce Thompson Institute for Plant Research; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; Argentina
Fil: Zhen, Yi. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Pombo, Marina Alejandra. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Zhong, Silin. Boyce Thompson Institute for Plant Research; Estados Unidos. University of Hong Kong; Hong Kong
Fil: Bombarely, Aureliano. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Fei, Zhangjun. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Collmer, Alan. Cornell University; Estados Unidos. King Abdulaziz University; Estados Unidos
Fil: Martin, Gregory B.. Boyce Thompson Institute for Plant Research; Estados Unidos. Cornell University; Estados Unidos. King Abdulaziz University; Estados Unidos
Materia
RNA-SEQ
PATTERN TRIGGERED IMMUNITY
PLANT IMMUNITY
TYPE III EFFECTORS
PSEUDOMONAS SYRINGAE
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/24275
Acceder
id CONICETDig_09b86f3be300009d86d33f73fc734711
oai_identifier_str oai:ri.conicet.gov.ar:11336/24275
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunityRosli, Hernan GuillermoZhen, YiPombo, Marina AlejandraZhong, SilinBombarely, AurelianoFei, ZhangjunCollmer, AlanMartin, Gregory B.RNA-SEQPATTERN TRIGGERED IMMUNITYPLANT IMMUNITYTYPE III EFFECTORSPSEUDOMONAS SYRINGAEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background: Microbe-associated molecular patterns, such as those present in bacterial flagellin, are powerful inducers of the innate immune response in plants. Successful pathogens deliver virulence proteins, termed effectors, into the plant cell where they can interfere with the immune response and promote disease. Engineering the plant immune system to enhance disease resistance requires a thorough understanding of its components. Results: We describe a high-throughput screen, using RNA sequencing and virus-induced gene silencing, to identify tomato genes whose expression is enhanced by the flagellin microbe-associated molecular pattern flgII-28, but reduced by activities of the Pseudomonas syringae pv. tomato (Pst) type III effectors AvrPto and AvrPtoB. Gene ontology terms for this category of Flagellin-induced repressed by effectors (FIRE) genes showed enrichment for genes encoding certain subfamilies of protein kinases and transcription factors. At least 25 of the FIRE genes have been implicated previously in plant immunity. Of the 92 protein kinase-encoding FIRE genes, 33 were subjected to virus-induced gene silencing and their involvement in pattern-triggered immunity was tested with a leaf-based assay. Silencing of one FIRE gene, which encodes the cell wall-associated kinase SlWAK1, compromised the plant immune response resulting in increased growth of Pst and enhanced disease symptoms. Conclusions: Our transcriptomic approach identifies FIRE genes that represent a pathogen-defined core set of immune-related genes. The analysis of this set of candidate genes led to the discovery of a cell wall-associated kinase that participates in plant defense. The FIRE genes will be useful for further elucidation of the plant immune system.Fil: Rosli, Hernan Guillermo. Boyce Thompson Institute for Plant Research; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Zhen, Yi. Boyce Thompson Institute for Plant Research; Estados UnidosFil: Pombo, Marina Alejandra. Boyce Thompson Institute for Plant Research; Estados UnidosFil: Zhong, Silin. Boyce Thompson Institute for Plant Research; Estados Unidos. University of Hong Kong; Hong KongFil: Bombarely, Aureliano. Boyce Thompson Institute for Plant Research; Estados UnidosFil: Fei, Zhangjun. Boyce Thompson Institute for Plant Research; Estados UnidosFil: Collmer, Alan. Cornell University; Estados Unidos. King Abdulaziz University; Estados UnidosFil: Martin, Gregory B.. Boyce Thompson Institute for Plant Research; Estados Unidos. Cornell University; Estados Unidos. King Abdulaziz University; Estados UnidosBioMed Central2013-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/24275Rosli, Hernan Guillermo; Zhen, Yi; Pombo, Marina Alejandra; Zhong, Silin; Bombarely, Aureliano; et al.; Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity; BioMed Central; Genome Biology; 14; 11-2013; 1-151474-760XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1186/gb-2013-14-12-r139info:eu-repo/semantics/altIdentifier/url/https://genomebiology.biomedcentral.com/articles/10.1186/gb-2013-14-12-r139info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:19:03Zoai:ri.conicet.gov.ar:11336/24275instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:19:03.307CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
title Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
spellingShingle Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
Rosli, Hernan Guillermo
RNA-SEQ
PATTERN TRIGGERED IMMUNITY
PLANT IMMUNITY
TYPE III EFFECTORS
PSEUDOMONAS SYRINGAE
title_short Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
title_full Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
title_fullStr Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
title_full_unstemmed Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
title_sort Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity
dc.creator.none.fl_str_mv Rosli, Hernan Guillermo
Zhen, Yi
Pombo, Marina Alejandra
Zhong, Silin
Bombarely, Aureliano
Fei, Zhangjun
Collmer, Alan
Martin, Gregory B.
author Rosli, Hernan Guillermo
author_facet Rosli, Hernan Guillermo
Zhen, Yi
Pombo, Marina Alejandra
Zhong, Silin
Bombarely, Aureliano
Fei, Zhangjun
Collmer, Alan
Martin, Gregory B.
author_role author
author2 Zhen, Yi
Pombo, Marina Alejandra
Zhong, Silin
Bombarely, Aureliano
Fei, Zhangjun
Collmer, Alan
Martin, Gregory B.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv RNA-SEQ
PATTERN TRIGGERED IMMUNITY
PLANT IMMUNITY
TYPE III EFFECTORS
PSEUDOMONAS SYRINGAE
topic RNA-SEQ
PATTERN TRIGGERED IMMUNITY
PLANT IMMUNITY
TYPE III EFFECTORS
PSEUDOMONAS SYRINGAE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background: Microbe-associated molecular patterns, such as those present in bacterial flagellin, are powerful inducers of the innate immune response in plants. Successful pathogens deliver virulence proteins, termed effectors, into the plant cell where they can interfere with the immune response and promote disease. Engineering the plant immune system to enhance disease resistance requires a thorough understanding of its components. Results: We describe a high-throughput screen, using RNA sequencing and virus-induced gene silencing, to identify tomato genes whose expression is enhanced by the flagellin microbe-associated molecular pattern flgII-28, but reduced by activities of the Pseudomonas syringae pv. tomato (Pst) type III effectors AvrPto and AvrPtoB. Gene ontology terms for this category of Flagellin-induced repressed by effectors (FIRE) genes showed enrichment for genes encoding certain subfamilies of protein kinases and transcription factors. At least 25 of the FIRE genes have been implicated previously in plant immunity. Of the 92 protein kinase-encoding FIRE genes, 33 were subjected to virus-induced gene silencing and their involvement in pattern-triggered immunity was tested with a leaf-based assay. Silencing of one FIRE gene, which encodes the cell wall-associated kinase SlWAK1, compromised the plant immune response resulting in increased growth of Pst and enhanced disease symptoms. Conclusions: Our transcriptomic approach identifies FIRE genes that represent a pathogen-defined core set of immune-related genes. The analysis of this set of candidate genes led to the discovery of a cell wall-associated kinase that participates in plant defense. The FIRE genes will be useful for further elucidation of the plant immune system.
Fil: Rosli, Hernan Guillermo. Boyce Thompson Institute for Plant Research; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; Argentina
Fil: Zhen, Yi. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Pombo, Marina Alejandra. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Zhong, Silin. Boyce Thompson Institute for Plant Research; Estados Unidos. University of Hong Kong; Hong Kong
Fil: Bombarely, Aureliano. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Fei, Zhangjun. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Collmer, Alan. Cornell University; Estados Unidos. King Abdulaziz University; Estados Unidos
Fil: Martin, Gregory B.. Boyce Thompson Institute for Plant Research; Estados Unidos. Cornell University; Estados Unidos. King Abdulaziz University; Estados Unidos
description Background: Microbe-associated molecular patterns, such as those present in bacterial flagellin, are powerful inducers of the innate immune response in plants. Successful pathogens deliver virulence proteins, termed effectors, into the plant cell where they can interfere with the immune response and promote disease. Engineering the plant immune system to enhance disease resistance requires a thorough understanding of its components. Results: We describe a high-throughput screen, using RNA sequencing and virus-induced gene silencing, to identify tomato genes whose expression is enhanced by the flagellin microbe-associated molecular pattern flgII-28, but reduced by activities of the Pseudomonas syringae pv. tomato (Pst) type III effectors AvrPto and AvrPtoB. Gene ontology terms for this category of Flagellin-induced repressed by effectors (FIRE) genes showed enrichment for genes encoding certain subfamilies of protein kinases and transcription factors. At least 25 of the FIRE genes have been implicated previously in plant immunity. Of the 92 protein kinase-encoding FIRE genes, 33 were subjected to virus-induced gene silencing and their involvement in pattern-triggered immunity was tested with a leaf-based assay. Silencing of one FIRE gene, which encodes the cell wall-associated kinase SlWAK1, compromised the plant immune response resulting in increased growth of Pst and enhanced disease symptoms. Conclusions: Our transcriptomic approach identifies FIRE genes that represent a pathogen-defined core set of immune-related genes. The analysis of this set of candidate genes led to the discovery of a cell wall-associated kinase that participates in plant defense. The FIRE genes will be useful for further elucidation of the plant immune system.
publishDate 2013
dc.date.none.fl_str_mv 2013-11
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/24275
Rosli, Hernan Guillermo; Zhen, Yi; Pombo, Marina Alejandra; Zhong, Silin; Bombarely, Aureliano; et al.; Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity; BioMed Central; Genome Biology; 14; 11-2013; 1-15
1474-760X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/24275
identifier_str_mv Rosli, Hernan Guillermo; Zhen, Yi; Pombo, Marina Alejandra; Zhong, Silin; Bombarely, Aureliano; et al.; Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity; BioMed Central; Genome Biology; 14; 11-2013; 1-15
1474-760X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1186/gb-2013-14-12-r139
info:eu-repo/semantics/altIdentifier/url/https://genomebiology.biomedcentral.com/articles/10.1186/gb-2013-14-12-r139
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 12.48226

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