Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid

Autores
Asai, Shuta; Rallapalli, Ganashyam; Piquerez, Sophie J. M.; Caillaud, Marie Cecile; Furzer, Oliver J.; Ishaque, Naveed; Wirthmueller, Lennart; Fabro, Georgina; Shirasu, Ken; Jones, Jonathan D. G.
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.
Fil: Asai, Shuta. Norwich Research Park. Norwich; Reino Unido. Center for Sustainable Resource Science. Kanagawa; Japón
Fil: Rallapalli, Ganashyam. Norwich Research Park. Norwich; Reino Unido
Fil: Piquerez, Sophie J. M.. Norwich Research Park. Norwich; Reino Unido
Fil: Caillaud, Marie Cecile. Norwich Research Park. Norwich; Reino Unido
Fil: Furzer, Oliver J.. Norwich Research Park. Norwich; Reino Unido
Fil: Ishaque, Naveed. Norwich Research Park. Norwich; Reino Unido
Fil: Wirthmueller, Lennart. Norwich Research Park. Norwich; Reino Unido
Fil: Fabro, Georgina. Norwich Research Park. Norwich; Reino Unido. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; Argentina
Fil: Shirasu, Ken. Center for Sustainable Resource Science. Kanagawa; Japón
Fil: Jones, Jonathan D. G.. Norwich Research Park. Norwich; Reino Unido
Materia
HYALOPERONOSPORA
TRANSCRIPTOME
SALICYLIC
DEFENCE
EFFECTOR
ARABIDOPSIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/32101
Acceder
id CONICETDig_d254cf3d32cc47513109eb472ffcdec6
oai_identifier_str oai:ri.conicet.gov.ar:11336/32101
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic AcidAsai, ShutaRallapalli, GanashyamPiquerez, Sophie J. M.Caillaud, Marie CecileFurzer, Oliver J.Ishaque, NaveedWirthmueller, LennartFabro, GeorginaShirasu, KenJones, Jonathan D. G.HYALOPERONOSPORATRANSCRIPTOMESALICYLICDEFENCEEFFECTORARABIDOPSIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.Fil: Asai, Shuta. Norwich Research Park. Norwich; Reino Unido. Center for Sustainable Resource Science. Kanagawa; JapónFil: Rallapalli, Ganashyam. Norwich Research Park. Norwich; Reino UnidoFil: Piquerez, Sophie J. M.. Norwich Research Park. Norwich; Reino UnidoFil: Caillaud, Marie Cecile. Norwich Research Park. Norwich; Reino UnidoFil: Furzer, Oliver J.. Norwich Research Park. Norwich; Reino UnidoFil: Ishaque, Naveed. Norwich Research Park. Norwich; Reino UnidoFil: Wirthmueller, Lennart. Norwich Research Park. Norwich; Reino UnidoFil: Fabro, Georgina. Norwich Research Park. Norwich; Reino Unido. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; ArgentinaFil: Shirasu, Ken. Center for Sustainable Resource Science. Kanagawa; JapónFil: Jones, Jonathan D. G.. Norwich Research Park. Norwich; Reino UnidoPublic Library of Science2014-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/32101Jones, Jonathan D. G.; Shirasu, Ken; Fabro, Georgina; Wirthmueller, Lennart; Ishaque, Naveed; Furzer, Oliver J.; et al.; Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid; Public Library of Science; Plos Pathogens; 10; 10-2014; 1-141553-7366CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1371/journal.ppat.1004443info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1004443info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:52:47Zoai:ri.conicet.gov.ar:11336/32101instacron: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:34982025-09-03 09:52:47.911CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
title Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
spellingShingle Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
Asai, Shuta
HYALOPERONOSPORA
TRANSCRIPTOME
SALICYLIC
DEFENCE
EFFECTOR
ARABIDOPSIS
title_short Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
title_full Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
title_fullStr Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
title_full_unstemmed Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
title_sort Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid
dc.creator.none.fl_str_mv Asai, Shuta
Rallapalli, Ganashyam
Piquerez, Sophie J. M.
Caillaud, Marie Cecile
Furzer, Oliver J.
Ishaque, Naveed
Wirthmueller, Lennart
Fabro, Georgina
Shirasu, Ken
Jones, Jonathan D. G.
author Asai, Shuta
author_facet Asai, Shuta
Rallapalli, Ganashyam
Piquerez, Sophie J. M.
Caillaud, Marie Cecile
Furzer, Oliver J.
Ishaque, Naveed
Wirthmueller, Lennart
Fabro, Georgina
Shirasu, Ken
Jones, Jonathan D. G.
author_role author
author2 Rallapalli, Ganashyam
Piquerez, Sophie J. M.
Caillaud, Marie Cecile
Furzer, Oliver J.
Ishaque, Naveed
Wirthmueller, Lennart
Fabro, Georgina
Shirasu, Ken
Jones, Jonathan D. G.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv HYALOPERONOSPORA
TRANSCRIPTOME
SALICYLIC
DEFENCE
EFFECTOR
ARABIDOPSIS
topic HYALOPERONOSPORA
TRANSCRIPTOME
SALICYLIC
DEFENCE
EFFECTOR
ARABIDOPSIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.
Fil: Asai, Shuta. Norwich Research Park. Norwich; Reino Unido. Center for Sustainable Resource Science. Kanagawa; Japón
Fil: Rallapalli, Ganashyam. Norwich Research Park. Norwich; Reino Unido
Fil: Piquerez, Sophie J. M.. Norwich Research Park. Norwich; Reino Unido
Fil: Caillaud, Marie Cecile. Norwich Research Park. Norwich; Reino Unido
Fil: Furzer, Oliver J.. Norwich Research Park. Norwich; Reino Unido
Fil: Ishaque, Naveed. Norwich Research Park. Norwich; Reino Unido
Fil: Wirthmueller, Lennart. Norwich Research Park. Norwich; Reino Unido
Fil: Fabro, Georgina. Norwich Research Park. Norwich; Reino Unido. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; Argentina
Fil: Shirasu, Ken. Center for Sustainable Resource Science. Kanagawa; Japón
Fil: Jones, Jonathan D. G.. Norwich Research Park. Norwich; Reino Unido
description Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.
publishDate 2014
dc.date.none.fl_str_mv 2014-10
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/11336/32101
Jones, Jonathan D. G.; Shirasu, Ken; Fabro, Georgina; Wirthmueller, Lennart; Ishaque, Naveed; Furzer, Oliver J.; et al.; Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid; Public Library of Science; Plos Pathogens; 10; 10-2014; 1-14
1553-7366
CONICET Digital
CONICET
url http://hdl.handle.net/11336/32101
identifier_str_mv Jones, Jonathan D. G.; Shirasu, Ken; Fabro, Georgina; Wirthmueller, Lennart; Ishaque, Naveed; Furzer, Oliver J.; et al.; Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid; Public Library of Science; Plos Pathogens; 10; 10-2014; 1-14
1553-7366
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.ppat.1004443
info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1004443
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
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
_version_ 1842269182794661888
score 13.13397

Publicaciones similares