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
- Institución
- Instituto Nacional de Tecnología Agropecuaria
- OAI Identificador
- oai:localhost:20.500.12123/8757
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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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12.559606 |