Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans

Autores
Savage, Zachary; Duggan, Cian; Toufexi, Alexia; Pandey, Pooja; Liang, Yuxi; Segretin, Maria Eugenia; Yuen, Lok Him; Gaboriau, David C. A.; Leary, Alexandre Y.; Tumtas, Yasin; Khandare, Virendrasinh; Ward, Andrew D.; Botchway, Stanley W.; Bateman, Benji C.; Pan, Indranil; Schattat, Martin; Sparkes, Imogen; Bozkurt, Osman Tolga
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1)-mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector-mediated suppression of BAK1-mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant–pathogen interactions.
Fil: Savage, Zachary. Imperial College London; Reino Unido
Fil: Duggan, Cian. Imperial College London; Reino Unido
Fil: Toufexi, Alexia. Imperial College London; Reino Unido
Fil: Pandey, Pooja. Imperial College London; Reino Unido
Fil: Liang, Yuxi. Imperial College London; Reino Unido
Fil: Segretin, Maria Eugenia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Yuen, Lok Him. Imperial College London; Reino Unido
Fil: Gaboriau, David C. A.. Imperial College London; Reino Unido
Fil: Leary, Alexandre Y.. Imperial College London; Reino Unido
Fil: Tumtas, Yasin. Imperial College London; Reino Unido
Fil: Khandare, Virendrasinh. Imperial College London; Reino Unido
Fil: Ward, Andrew D.. Science and Technology Facilities Council; Reino Unido
Fil: Botchway, Stanley W.. Science and Technology Facilities Council; Reino Unido
Fil: Bateman, Benji C.. Science and Technology Facilities Council; Reino Unido
Fil: Pan, Indranil. Alan Turing Institute; Reino Unido. Imperial College London; Reino Unido
Fil: Schattat, Martin. Martin Luther Universitat Halle-Wittenberg; Alemania
Fil: Sparkes, Imogen. University of Bristol; Reino Unido
Fil: Bozkurt, Osman Tolga. Imperial College London; Reino Unido
Materia
CHLOROPLAST MOVEMENT
EFFECTORS
FOCAL IMMUNITY
HAUSTORIUM
LASER CAPTURE
PHYTOPHTHORA INFESTANS
STROMULE
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:11336/153128
Acceder
id CONICETDig_30c5583cce42e133545616fee9217eb9
oai_identifier_str oai:ri.conicet.gov.ar:11336/153128
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestansSavage, ZacharyDuggan, CianToufexi, AlexiaPandey, PoojaLiang, YuxiSegretin, Maria EugeniaYuen, Lok HimGaboriau, David C. A.Leary, Alexandre Y.Tumtas, YasinKhandare, VirendrasinhWard, Andrew D.Botchway, Stanley W.Bateman, Benji C.Pan, IndranilSchattat, MartinSparkes, ImogenBozkurt, Osman TolgaCHLOROPLAST MOVEMENTEFFECTORSFOCAL IMMUNITYHAUSTORIUMLASER CAPTUREPHYTOPHTHORA INFESTANSSTROMULEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1)-mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector-mediated suppression of BAK1-mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant–pathogen interactions.Fil: Savage, Zachary. Imperial College London; Reino UnidoFil: Duggan, Cian. Imperial College London; Reino UnidoFil: Toufexi, Alexia. Imperial College London; Reino UnidoFil: Pandey, Pooja. Imperial College London; Reino UnidoFil: Liang, Yuxi. Imperial College London; Reino UnidoFil: Segretin, Maria Eugenia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Yuen, Lok Him. Imperial College London; Reino UnidoFil: Gaboriau, David C. A.. Imperial College London; Reino UnidoFil: Leary, Alexandre Y.. Imperial College London; Reino UnidoFil: Tumtas, Yasin. Imperial College London; Reino UnidoFil: Khandare, Virendrasinh. Imperial College London; Reino UnidoFil: Ward, Andrew D.. Science and Technology Facilities Council; Reino UnidoFil: Botchway, Stanley W.. Science and Technology Facilities Council; Reino UnidoFil: Bateman, Benji C.. Science and Technology Facilities Council; Reino UnidoFil: Pan, Indranil. Alan Turing Institute; Reino Unido. Imperial College London; Reino UnidoFil: Schattat, Martin. Martin Luther Universitat Halle-Wittenberg; AlemaniaFil: Sparkes, Imogen. University of Bristol; Reino UnidoFil: Bozkurt, Osman Tolga. Imperial College London; Reino UnidoWiley Blackwell Publishing, Inc2021-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/153128Savage, Zachary; Duggan, Cian; Toufexi, Alexia; Pandey, Pooja; Liang, Yuxi; et al.; Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans; Wiley Blackwell Publishing, Inc; Plant Journal; 107; 6; 9-2021; 1771-17870960-7412CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/tpj.15416info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1111/tpj.15416info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:56:08Zoai:ri.conicet.gov.ar:11336/153128instacron: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 09:56:08.658CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
title Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
spellingShingle Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
Savage, Zachary
CHLOROPLAST MOVEMENT
EFFECTORS
FOCAL IMMUNITY
HAUSTORIUM
LASER CAPTURE
PHYTOPHTHORA INFESTANS
STROMULE
title_short Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
title_full Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
title_fullStr Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
title_full_unstemmed Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
title_sort Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans
dc.creator.none.fl_str_mv Savage, Zachary
Duggan, Cian
Toufexi, Alexia
Pandey, Pooja
Liang, Yuxi
Segretin, Maria Eugenia
Yuen, Lok Him
Gaboriau, David C. A.
Leary, Alexandre Y.
Tumtas, Yasin
Khandare, Virendrasinh
Ward, Andrew D.
Botchway, Stanley W.
Bateman, Benji C.
Pan, Indranil
Schattat, Martin
Sparkes, Imogen
Bozkurt, Osman Tolga
author Savage, Zachary
author_facet Savage, Zachary
Duggan, Cian
Toufexi, Alexia
Pandey, Pooja
Liang, Yuxi
Segretin, Maria Eugenia
Yuen, Lok Him
Gaboriau, David C. A.
Leary, Alexandre Y.
Tumtas, Yasin
Khandare, Virendrasinh
Ward, Andrew D.
Botchway, Stanley W.
Bateman, Benji C.
Pan, Indranil
Schattat, Martin
Sparkes, Imogen
Bozkurt, Osman Tolga
author_role author
author2 Duggan, Cian
Toufexi, Alexia
Pandey, Pooja
Liang, Yuxi
Segretin, Maria Eugenia
Yuen, Lok Him
Gaboriau, David C. A.
Leary, Alexandre Y.
Tumtas, Yasin
Khandare, Virendrasinh
Ward, Andrew D.
Botchway, Stanley W.
Bateman, Benji C.
Pan, Indranil
Schattat, Martin
Sparkes, Imogen
Bozkurt, Osman Tolga
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CHLOROPLAST MOVEMENT
EFFECTORS
FOCAL IMMUNITY
HAUSTORIUM
LASER CAPTURE
PHYTOPHTHORA INFESTANS
STROMULE
topic CHLOROPLAST MOVEMENT
EFFECTORS
FOCAL IMMUNITY
HAUSTORIUM
LASER CAPTURE
PHYTOPHTHORA INFESTANS
STROMULE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1)-mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector-mediated suppression of BAK1-mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant–pathogen interactions.
Fil: Savage, Zachary. Imperial College London; Reino Unido
Fil: Duggan, Cian. Imperial College London; Reino Unido
Fil: Toufexi, Alexia. Imperial College London; Reino Unido
Fil: Pandey, Pooja. Imperial College London; Reino Unido
Fil: Liang, Yuxi. Imperial College London; Reino Unido
Fil: Segretin, Maria Eugenia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Yuen, Lok Him. Imperial College London; Reino Unido
Fil: Gaboriau, David C. A.. Imperial College London; Reino Unido
Fil: Leary, Alexandre Y.. Imperial College London; Reino Unido
Fil: Tumtas, Yasin. Imperial College London; Reino Unido
Fil: Khandare, Virendrasinh. Imperial College London; Reino Unido
Fil: Ward, Andrew D.. Science and Technology Facilities Council; Reino Unido
Fil: Botchway, Stanley W.. Science and Technology Facilities Council; Reino Unido
Fil: Bateman, Benji C.. Science and Technology Facilities Council; Reino Unido
Fil: Pan, Indranil. Alan Turing Institute; Reino Unido. Imperial College London; Reino Unido
Fil: Schattat, Martin. Martin Luther Universitat Halle-Wittenberg; Alemania
Fil: Sparkes, Imogen. University of Bristol; Reino Unido
Fil: Bozkurt, Osman Tolga. Imperial College London; Reino Unido
description Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1)-mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector-mediated suppression of BAK1-mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant–pathogen interactions.
publishDate 2021
dc.date.none.fl_str_mv 2021-09
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/11336/153128
Savage, Zachary; Duggan, Cian; Toufexi, Alexia; Pandey, Pooja; Liang, Yuxi; et al.; Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans; Wiley Blackwell Publishing, Inc; Plant Journal; 107; 6; 9-2021; 1771-1787
0960-7412
CONICET Digital
CONICET
url http://hdl.handle.net/11336/153128
identifier_str_mv Savage, Zachary; Duggan, Cian; Toufexi, Alexia; Pandey, Pooja; Liang, Yuxi; et al.; Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans; Wiley Blackwell Publishing, Inc; Plant Journal; 107; 6; 9-2021; 1771-1787
0960-7412
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/tpj.15416
info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1111/tpj.15416
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 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
_version_ 1842269386531930112
score 13.13397

Publicaciones similares