Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots

Autores
Robert, German; Yagyu, Mako; Koizumi, Takaya; Naya, Loreto; Masclaux‐Daubresse, Céline; Yoshimoto, Kohki
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Plant responses to NH4 + stress are complex, and multiple mechanisms underlying NH4 + sensitivity and tolerance in plants may be involved. Here, we demonstrate that macro‐ and microautophagic activities are oppositely affected in plants grown under NH4 + toxicity conditions. When grown under NH4 + stress conditions, macroautophagic activity was impaired in roots. Root cells accumulated autophagosomes in the cytoplasm, but showed less autophagic flux, indicating that late steps of the macroautophagy process are affected under NH4 + stress conditions. Under this scenario, we also found that the CCZ1‐MON1 complex, a critical factor for vacuole delivery pathways, functions in the late step of the macroautophagic pathway in Arabidopsis. In contrast, an accumulation of tonoplast‐derived vesicles was observed in vacuolar lumens of root cells of NH4 +‐stressed plants, suggesting the induction of a microautophagy‐like process. In this sense, some SYP22‐, but mainly VAMP711‐positive vesicles were observed inside vacuole in roots of NH4 +‐stressed plants. Consistent with the increased tonoplast degradation and the reduced membrane flow to the vacuole due to the impaired macroautophagic flux, the vacuoles of root cells of NH4 +‐stressed plants showed a simplified structure and lower tonoplast content. Taken together, this study presents evidence that postulates late steps of the macroautophagic process as a relevant physiological mechanism underlying the NH4 + sensitivity response in Arabidopsis, and additionally provides insights into the molecular tools for studying microautophagy in plants.
Instituto de Fisiología y Recursos Genéticos Vegetales
Fil: Robert, German. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Unidad de Estudios Agropecuarios (UDEA); Argentina. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; France
Fil: Yagyu, Mako. Meiji University. School of Agriculture. Department of Life Sciences; Japón
Fil: Koizumi, Takaya. Meiji University. School of Agriculture. Department of Life Sciences; Japón
Fil: Naya, Loreto. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia
Fil: Masclaux‐Daubresse, Céline. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia
Fil: Yoshimoto, Kohki. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia. Meiji University. School of Agriculture. Department of Life Sciences; Japón
Fuente
The Plant Journal 105 (4) : 1083-1097 (February 2021)
Materia
Ammonium Nitrogen
Toxicity
Vacuoles
Stress
Arabidopsis
Nitrógeno Amoniacal
Toxicidad
Vacúola
Estres
NH4-N
NH4
CCZ1-MON1
Macroautophagy
Microautophagy
Autophagosome-to-vacuole Fusion
Vacuole Morphology
Nivel de accesibilidad
acceso restringido
Condiciones de uso
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
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oai_identifier_str oai:localhost:20.500.12123/8757
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network_name_str INTA Digital (INTA)
spelling Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis rootsRobert, GermanYagyu, MakoKoizumi, TakayaNaya, LoretoMasclaux‐Daubresse, CélineYoshimoto, KohkiAmmonium NitrogenToxicityVacuolesStressArabidopsisNitrógeno AmoniacalToxicidadVacúolaEstresNH4-NNH4CCZ1-MON1MacroautophagyMicroautophagyAutophagosome-to-vacuole FusionVacuole MorphologyPlant responses to NH4 + stress are complex, and multiple mechanisms underlying NH4 + sensitivity and tolerance in plants may be involved. Here, we demonstrate that macro‐ and microautophagic activities are oppositely affected in plants grown under NH4 + toxicity conditions. When grown under NH4 + stress conditions, macroautophagic activity was impaired in roots. Root cells accumulated autophagosomes in the cytoplasm, but showed less autophagic flux, indicating that late steps of the macroautophagy process are affected under NH4 + stress conditions. Under this scenario, we also found that the CCZ1‐MON1 complex, a critical factor for vacuole delivery pathways, functions in the late step of the macroautophagic pathway in Arabidopsis. In contrast, an accumulation of tonoplast‐derived vesicles was observed in vacuolar lumens of root cells of NH4 +‐stressed plants, suggesting the induction of a microautophagy‐like process. In this sense, some SYP22‐, but mainly VAMP711‐positive vesicles were observed inside vacuole in roots of NH4 +‐stressed plants. Consistent with the increased tonoplast degradation and the reduced membrane flow to the vacuole due to the impaired macroautophagic flux, the vacuoles of root cells of NH4 +‐stressed plants showed a simplified structure and lower tonoplast content. Taken together, this study presents evidence that postulates late steps of the macroautophagic process as a relevant physiological mechanism underlying the NH4 + sensitivity response in Arabidopsis, and additionally provides insights into the molecular tools for studying microautophagy in plants.Instituto de Fisiología y Recursos Genéticos VegetalesFil: Robert, German. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Unidad de Estudios Agropecuarios (UDEA); Argentina. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; FranceFil: Yagyu, Mako. Meiji University. School of Agriculture. Department of Life Sciences; JapónFil: Koizumi, Takaya. Meiji University. School of Agriculture. Department of Life Sciences; JapónFil: Naya, Loreto. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; FranciaFil: Masclaux‐Daubresse, Céline. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; FranciaFil: Yoshimoto, Kohki. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia. Meiji University. School of Agriculture. Department of Life Sciences; JapónWiley2021-02-26T11:39:46Z2021-02-26T11:39:46Z2020-11-22info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/8757https://onlinelibrary.wiley.com/doi/10.1111/tpj.150910960-74121365-313X (online)https://doi.org/10.1111/tpj.15091The Plant Journal 105 (4) : 1083-1097 (February 2021)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/restrictedAccess2025-09-29T13:45:08Zoai:localhost:20.500.12123/8757instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-29 13:45:08.652INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
title Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
spellingShingle Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
Robert, German
Ammonium Nitrogen
Toxicity
Vacuoles
Stress
Arabidopsis
Nitrógeno Amoniacal
Toxicidad
Vacúola
Estres
NH4-N
NH4
CCZ1-MON1
Macroautophagy
Microautophagy
Autophagosome-to-vacuole Fusion
Vacuole Morphology
title_short Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
title_full Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
title_fullStr Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
title_full_unstemmed Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
title_sort Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
dc.creator.none.fl_str_mv Robert, German
Yagyu, Mako
Koizumi, Takaya
Naya, Loreto
Masclaux‐Daubresse, Céline
Yoshimoto, Kohki
author Robert, German
author_facet Robert, German
Yagyu, Mako
Koizumi, Takaya
Naya, Loreto
Masclaux‐Daubresse, Céline
Yoshimoto, Kohki
author_role author
author2 Yagyu, Mako
Koizumi, Takaya
Naya, Loreto
Masclaux‐Daubresse, Céline
Yoshimoto, Kohki
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Ammonium Nitrogen
Toxicity
Vacuoles
Stress
Arabidopsis
Nitrógeno Amoniacal
Toxicidad
Vacúola
Estres
NH4-N
NH4
CCZ1-MON1
Macroautophagy
Microautophagy
Autophagosome-to-vacuole Fusion
Vacuole Morphology
topic Ammonium Nitrogen
Toxicity
Vacuoles
Stress
Arabidopsis
Nitrógeno Amoniacal
Toxicidad
Vacúola
Estres
NH4-N
NH4
CCZ1-MON1
Macroautophagy
Microautophagy
Autophagosome-to-vacuole Fusion
Vacuole Morphology
dc.description.none.fl_txt_mv Plant responses to NH4 + stress are complex, and multiple mechanisms underlying NH4 + sensitivity and tolerance in plants may be involved. Here, we demonstrate that macro‐ and microautophagic activities are oppositely affected in plants grown under NH4 + toxicity conditions. When grown under NH4 + stress conditions, macroautophagic activity was impaired in roots. Root cells accumulated autophagosomes in the cytoplasm, but showed less autophagic flux, indicating that late steps of the macroautophagy process are affected under NH4 + stress conditions. Under this scenario, we also found that the CCZ1‐MON1 complex, a critical factor for vacuole delivery pathways, functions in the late step of the macroautophagic pathway in Arabidopsis. In contrast, an accumulation of tonoplast‐derived vesicles was observed in vacuolar lumens of root cells of NH4 +‐stressed plants, suggesting the induction of a microautophagy‐like process. In this sense, some SYP22‐, but mainly VAMP711‐positive vesicles were observed inside vacuole in roots of NH4 +‐stressed plants. Consistent with the increased tonoplast degradation and the reduced membrane flow to the vacuole due to the impaired macroautophagic flux, the vacuoles of root cells of NH4 +‐stressed plants showed a simplified structure and lower tonoplast content. Taken together, this study presents evidence that postulates late steps of the macroautophagic process as a relevant physiological mechanism underlying the NH4 + sensitivity response in Arabidopsis, and additionally provides insights into the molecular tools for studying microautophagy in plants.
Instituto de Fisiología y Recursos Genéticos Vegetales
Fil: Robert, German. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Unidad de Estudios Agropecuarios (UDEA); Argentina. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; France
Fil: Yagyu, Mako. Meiji University. School of Agriculture. Department of Life Sciences; Japón
Fil: Koizumi, Takaya. Meiji University. School of Agriculture. Department of Life Sciences; Japón
Fil: Naya, Loreto. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia
Fil: Masclaux‐Daubresse, Céline. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia
Fil: Yoshimoto, Kohki. Université Paris‐Saclay. Institut Jean‐Pierre Bourgin, INRAE, AgroParisTech; Francia. Meiji University. School of Agriculture. Department of Life Sciences; Japón
description Plant responses to NH4 + stress are complex, and multiple mechanisms underlying NH4 + sensitivity and tolerance in plants may be involved. Here, we demonstrate that macro‐ and microautophagic activities are oppositely affected in plants grown under NH4 + toxicity conditions. When grown under NH4 + stress conditions, macroautophagic activity was impaired in roots. Root cells accumulated autophagosomes in the cytoplasm, but showed less autophagic flux, indicating that late steps of the macroautophagy process are affected under NH4 + stress conditions. Under this scenario, we also found that the CCZ1‐MON1 complex, a critical factor for vacuole delivery pathways, functions in the late step of the macroautophagic pathway in Arabidopsis. In contrast, an accumulation of tonoplast‐derived vesicles was observed in vacuolar lumens of root cells of NH4 +‐stressed plants, suggesting the induction of a microautophagy‐like process. In this sense, some SYP22‐, but mainly VAMP711‐positive vesicles were observed inside vacuole in roots of NH4 +‐stressed plants. Consistent with the increased tonoplast degradation and the reduced membrane flow to the vacuole due to the impaired macroautophagic flux, the vacuoles of root cells of NH4 +‐stressed plants showed a simplified structure and lower tonoplast content. Taken together, this study presents evidence that postulates late steps of the macroautophagic process as a relevant physiological mechanism underlying the NH4 + sensitivity response in Arabidopsis, and additionally provides insights into the molecular tools for studying microautophagy in plants.
publishDate 2020
dc.date.none.fl_str_mv 2020-11-22
2021-02-26T11:39:46Z
2021-02-26T11:39:46Z
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/20.500.12123/8757
https://onlinelibrary.wiley.com/doi/10.1111/tpj.15091
0960-7412
1365-313X (online)
https://doi.org/10.1111/tpj.15091
url http://hdl.handle.net/20.500.12123/8757
https://onlinelibrary.wiley.com/doi/10.1111/tpj.15091
https://doi.org/10.1111/tpj.15091
identifier_str_mv 0960-7412
1365-313X (online)
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/restrictedAccess
eu_rights_str_mv restrictedAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Wiley
publisher.none.fl_str_mv Wiley
dc.source.none.fl_str_mv The Plant Journal 105 (4) : 1083-1097 (February 2021)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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