Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1

Autores
Wirthmueller, Lennart; Asai, Shuta; Rallapalli, Ghanasyam; Sklenar, Jan; Fabro, Georgina; Kim, Dae Sung; Lintermann, Ruth; Jaspers, Pinja; Wrzaczek, Michael; Kangasjärvi, Jaakko; MacLean, Daniel; Menke, Frank L. H.; Banfield, Mark J.; Jones, Jonathan D. G.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL-INDUCED CELL DEATH1 (RCD1). We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes. We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)-induced defense genes and alters plant growth responses to light. HaRxL106-mediated suppression of immunity is abolished in RCD1 loss-of-function mutants. We report that RCD1-type proteins are phosphorylated, and we identified Mut9-like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1-interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared with wild-type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling. Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.
Fil: Wirthmueller, Lennart. Freie Universität Berlin; Alemania
Fil: Asai, Shuta. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Rallapalli, Ghanasyam. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Sklenar, Jan. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Fabro, Georgina. 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: Kim, Dae Sung. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Lintermann, Ruth. Freie Universität Berlin; Alemania
Fil: Jaspers, Pinja. University of Helsinki; Finlandia
Fil: Wrzaczek, Michael. University of Helsinki; Finlandia
Fil: Kangasjärvi, Jaakko. University of Helsinki; Finlandia
Fil: MacLean, Daniel. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Menke, Frank L. H.. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Banfield, Mark J.. John Innes Institute; Reino Unido
Fil: Jones, Jonathan D. G.. The Sainsbury Laboratory Norwich; Reino Unido
Materia
ARABIDOPSIS THALIANA
HYALOPERONOSPORA ARABIDOPSIDIS
OOMYCETE PATHOGEN
PATHOGEN EFFECTOR
PLANT INNATE IMMUNITY
RADICAL-INDUCED CELL DEATH1
SALICYLIC ACID (SA)
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:11336/129657
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/129657
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1Wirthmueller, LennartAsai, ShutaRallapalli, GhanasyamSklenar, JanFabro, GeorginaKim, Dae SungLintermann, RuthJaspers, PinjaWrzaczek, MichaelKangasjärvi, JaakkoMacLean, DanielMenke, Frank L. H.Banfield, Mark J.Jones, Jonathan D. G.ARABIDOPSIS THALIANAHYALOPERONOSPORA ARABIDOPSIDISOOMYCETE PATHOGENPATHOGEN EFFECTORPLANT INNATE IMMUNITYRADICAL-INDUCED CELL DEATH1SALICYLIC ACID (SA)https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL-INDUCED CELL DEATH1 (RCD1). We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes. We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)-induced defense genes and alters plant growth responses to light. HaRxL106-mediated suppression of immunity is abolished in RCD1 loss-of-function mutants. We report that RCD1-type proteins are phosphorylated, and we identified Mut9-like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1-interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared with wild-type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling. Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.Fil: Wirthmueller, Lennart. Freie Universität Berlin; AlemaniaFil: Asai, Shuta. The Sainsbury Laboratory Norwich; Reino UnidoFil: Rallapalli, Ghanasyam. The Sainsbury Laboratory Norwich; Reino UnidoFil: Sklenar, Jan. The Sainsbury Laboratory Norwich; Reino UnidoFil: Fabro, Georgina. 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: Kim, Dae Sung. The Sainsbury Laboratory Norwich; Reino UnidoFil: Lintermann, Ruth. Freie Universität Berlin; AlemaniaFil: Jaspers, Pinja. University of Helsinki; FinlandiaFil: Wrzaczek, Michael. University of Helsinki; FinlandiaFil: Kangasjärvi, Jaakko. University of Helsinki; FinlandiaFil: MacLean, Daniel. The Sainsbury Laboratory Norwich; Reino UnidoFil: Menke, Frank L. H.. The Sainsbury Laboratory Norwich; Reino UnidoFil: Banfield, Mark J.. John Innes Institute; Reino UnidoFil: Jones, Jonathan D. G.. The Sainsbury Laboratory Norwich; Reino UnidoWiley Blackwell Publishing, Inc2018-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/129657Wirthmueller, Lennart; Asai, Shuta; Rallapalli, Ghanasyam; Sklenar, Jan; Fabro, Georgina; et al.; Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1; Wiley Blackwell Publishing, Inc; New Phytologist; 220; 1; 10-2018; 232-2480028-646X1469-8137CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/ 10.1111/nph.15277info:eu-repo/semantics/altIdentifier/url/https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.15277info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:07:52Zoai:ri.conicet.gov.ar:11336/129657instacron: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 13:07:52.32CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
title Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
spellingShingle Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
Wirthmueller, Lennart
ARABIDOPSIS THALIANA
HYALOPERONOSPORA ARABIDOPSIDIS
OOMYCETE PATHOGEN
PATHOGEN EFFECTOR
PLANT INNATE IMMUNITY
RADICAL-INDUCED CELL DEATH1
SALICYLIC ACID (SA)
title_short Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
title_full Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
title_fullStr Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
title_full_unstemmed Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
title_sort Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1
dc.creator.none.fl_str_mv Wirthmueller, Lennart
Asai, Shuta
Rallapalli, Ghanasyam
Sklenar, Jan
Fabro, Georgina
Kim, Dae Sung
Lintermann, Ruth
Jaspers, Pinja
Wrzaczek, Michael
Kangasjärvi, Jaakko
MacLean, Daniel
Menke, Frank L. H.
Banfield, Mark J.
Jones, Jonathan D. G.
author Wirthmueller, Lennart
author_facet Wirthmueller, Lennart
Asai, Shuta
Rallapalli, Ghanasyam
Sklenar, Jan
Fabro, Georgina
Kim, Dae Sung
Lintermann, Ruth
Jaspers, Pinja
Wrzaczek, Michael
Kangasjärvi, Jaakko
MacLean, Daniel
Menke, Frank L. H.
Banfield, Mark J.
Jones, Jonathan D. G.
author_role author
author2 Asai, Shuta
Rallapalli, Ghanasyam
Sklenar, Jan
Fabro, Georgina
Kim, Dae Sung
Lintermann, Ruth
Jaspers, Pinja
Wrzaczek, Michael
Kangasjärvi, Jaakko
MacLean, Daniel
Menke, Frank L. H.
Banfield, Mark J.
Jones, Jonathan D. G.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ARABIDOPSIS THALIANA
HYALOPERONOSPORA ARABIDOPSIDIS
OOMYCETE PATHOGEN
PATHOGEN EFFECTOR
PLANT INNATE IMMUNITY
RADICAL-INDUCED CELL DEATH1
SALICYLIC ACID (SA)
topic ARABIDOPSIS THALIANA
HYALOPERONOSPORA ARABIDOPSIDIS
OOMYCETE PATHOGEN
PATHOGEN EFFECTOR
PLANT INNATE IMMUNITY
RADICAL-INDUCED CELL DEATH1
SALICYLIC ACID (SA)
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL-INDUCED CELL DEATH1 (RCD1). We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes. We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)-induced defense genes and alters plant growth responses to light. HaRxL106-mediated suppression of immunity is abolished in RCD1 loss-of-function mutants. We report that RCD1-type proteins are phosphorylated, and we identified Mut9-like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1-interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared with wild-type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling. Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.
Fil: Wirthmueller, Lennart. Freie Universität Berlin; Alemania
Fil: Asai, Shuta. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Rallapalli, Ghanasyam. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Sklenar, Jan. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Fabro, Georgina. 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: Kim, Dae Sung. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Lintermann, Ruth. Freie Universität Berlin; Alemania
Fil: Jaspers, Pinja. University of Helsinki; Finlandia
Fil: Wrzaczek, Michael. University of Helsinki; Finlandia
Fil: Kangasjärvi, Jaakko. University of Helsinki; Finlandia
Fil: MacLean, Daniel. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Menke, Frank L. H.. The Sainsbury Laboratory Norwich; Reino Unido
Fil: Banfield, Mark J.. John Innes Institute; Reino Unido
Fil: Jones, Jonathan D. G.. The Sainsbury Laboratory Norwich; Reino Unido
description The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL-INDUCED CELL DEATH1 (RCD1). We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes. We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)-induced defense genes and alters plant growth responses to light. HaRxL106-mediated suppression of immunity is abolished in RCD1 loss-of-function mutants. We report that RCD1-type proteins are phosphorylated, and we identified Mut9-like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1-interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared with wild-type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling. Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.
publishDate 2018
dc.date.none.fl_str_mv 2018-10
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/11336/129657
Wirthmueller, Lennart; Asai, Shuta; Rallapalli, Ghanasyam; Sklenar, Jan; Fabro, Georgina; et al.; Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1; Wiley Blackwell Publishing, Inc; New Phytologist; 220; 1; 10-2018; 232-248
0028-646X
1469-8137
CONICET Digital
CONICET
url http://hdl.handle.net/11336/129657
identifier_str_mv Wirthmueller, Lennart; Asai, Shuta; Rallapalli, Ghanasyam; Sklenar, Jan; Fabro, Georgina; et al.; Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to radical-induced cell death1; Wiley Blackwell Publishing, Inc; New Phytologist; 220; 1; 10-2018; 232-248
0028-646X
1469-8137
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/ 10.1111/nph.15277
info:eu-repo/semantics/altIdentifier/url/https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.15277
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 Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
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 12.993085

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