Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria

Autores
Pierella Karlusich, Juan José; Zurbriggen, Matias Daniel; Shahinnia, Fahimeh; Sonnewald, Sophia; Sonnewald, Uwe; Hosseini, Seyed A.; Hajirezaei, Mohammad-Reza; Carrillo, Nestor Jose
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses.
Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Zurbriggen, Matias Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Shahinnia, Fahimeh. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Sonnewald, Sophia. Friedrich-Alexander-University Erlangen-Nuremberg; Alemania
Fil: Sonnewald, Uwe. Friedrich-Alexander-University Erlangen-Nuremberg; Alemania
Fil: Hosseini, Seyed A.. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Hajirezaei, Mohammad-Reza. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Materia
CHLOROPLAST REDOX STATUS
FLAVODOXIN
LOCALIZED CELL DEATH
PLANT-MICROBE INTERACTIONS
REACTIVE OXYGEN SPECIES
TRANSCRIPTOMICS
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:11336/52587

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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. VesicatoriaPierella Karlusich, Juan JoséZurbriggen, Matias DanielShahinnia, FahimehSonnewald, SophiaSonnewald, UweHosseini, Seyed A.Hajirezaei, Mohammad-RezaCarrillo, Nestor JoseCHLOROPLAST REDOX STATUSFLAVODOXINLOCALIZED CELL DEATHPLANT-MICROBE INTERACTIONSREACTIVE OXYGEN SPECIESTRANSCRIPTOMICShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses.Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Zurbriggen, Matias Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Shahinnia, Fahimeh. Leibniz Institute of Plant Genetics and Crop Plant Research; AlemaniaFil: Sonnewald, Sophia. Friedrich-Alexander-University Erlangen-Nuremberg; AlemaniaFil: Sonnewald, Uwe. Friedrich-Alexander-University Erlangen-Nuremberg; AlemaniaFil: Hosseini, Seyed A.. Leibniz Institute of Plant Genetics and Crop Plant Research; AlemaniaFil: Hajirezaei, Mohammad-Reza. Leibniz Institute of Plant Genetics and Crop Plant Research; AlemaniaFil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFrontiers Media S.A.2017-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/52587Pierella Karlusich, Juan José; Zurbriggen, Matias Daniel; Shahinnia, Fahimeh; Sonnewald, Sophia; Sonnewald, Uwe; et al.; Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria; Frontiers Media S.A.; Frontiers in Plant Science; 8; 7-2017; 1-211664-462XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.3389/fpls.2017.01158info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fpls.2017.01158/fullinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:52:51Zoai:ri.conicet.gov.ar:11336/52587instacron: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 09:52:51.603CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
title Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
spellingShingle Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
Pierella Karlusich, Juan José
CHLOROPLAST REDOX STATUS
FLAVODOXIN
LOCALIZED CELL DEATH
PLANT-MICROBE INTERACTIONS
REACTIVE OXYGEN SPECIES
TRANSCRIPTOMICS
title_short Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
title_full Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
title_fullStr Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
title_full_unstemmed Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
title_sort Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria
dc.creator.none.fl_str_mv Pierella Karlusich, Juan José
Zurbriggen, Matias Daniel
Shahinnia, Fahimeh
Sonnewald, Sophia
Sonnewald, Uwe
Hosseini, Seyed A.
Hajirezaei, Mohammad-Reza
Carrillo, Nestor Jose
author Pierella Karlusich, Juan José
author_facet Pierella Karlusich, Juan José
Zurbriggen, Matias Daniel
Shahinnia, Fahimeh
Sonnewald, Sophia
Sonnewald, Uwe
Hosseini, Seyed A.
Hajirezaei, Mohammad-Reza
Carrillo, Nestor Jose
author_role author
author2 Zurbriggen, Matias Daniel
Shahinnia, Fahimeh
Sonnewald, Sophia
Sonnewald, Uwe
Hosseini, Seyed A.
Hajirezaei, Mohammad-Reza
Carrillo, Nestor Jose
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CHLOROPLAST REDOX STATUS
FLAVODOXIN
LOCALIZED CELL DEATH
PLANT-MICROBE INTERACTIONS
REACTIVE OXYGEN SPECIES
TRANSCRIPTOMICS
topic CHLOROPLAST REDOX STATUS
FLAVODOXIN
LOCALIZED CELL DEATH
PLANT-MICROBE INTERACTIONS
REACTIVE OXYGEN SPECIES
TRANSCRIPTOMICS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses.
Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Zurbriggen, Matias Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Shahinnia, Fahimeh. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Sonnewald, Sophia. Friedrich-Alexander-University Erlangen-Nuremberg; Alemania
Fil: Sonnewald, Uwe. Friedrich-Alexander-University Erlangen-Nuremberg; Alemania
Fil: Hosseini, Seyed A.. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Hajirezaei, Mohammad-Reza. Leibniz Institute of Plant Genetics and Crop Plant Research; Alemania
Fil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
description Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses.
publishDate 2017
dc.date.none.fl_str_mv 2017-07
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/11336/52587
Pierella Karlusich, Juan José; Zurbriggen, Matias Daniel; Shahinnia, Fahimeh; Sonnewald, Sophia; Sonnewald, Uwe; et al.; Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria; Frontiers Media S.A.; Frontiers in Plant Science; 8; 7-2017; 1-21
1664-462X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/52587
identifier_str_mv Pierella Karlusich, Juan José; Zurbriggen, Matias Daniel; Shahinnia, Fahimeh; Sonnewald, Sophia; Sonnewald, Uwe; et al.; Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of Tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. Vesicatoria; Frontiers Media S.A.; Frontiers in Plant Science; 8; 7-2017; 1-21
1664-462X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.3389/fpls.2017.01158
info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fpls.2017.01158/full
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 Frontiers Media S.A.
publisher.none.fl_str_mv Frontiers Media S.A.
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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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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