Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots
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 + s...
| Autores principales: | , , , , , |
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| Formato: | Artículo |
| Lenguaje: | Inglés |
| Publicado: |
Wiley
2021
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| Materias: | |
| Acceso en línea: | http://hdl.handle.net/20.500.12123/8757 https://onlinelibrary.wiley.com/doi/10.1111/tpj.15091 https://doi.org/10.1111/tpj.15091 |
| _version_ | 1855484261875843072 |
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| author | Robert, German Yagyu, Mako Koizumi, Takaya Naya, Loreto Masclaux‐Daubresse, Céline Yoshimoto, Kohki |
| author_browse | Koizumi, Takaya Masclaux‐Daubresse, Céline Naya, Loreto Robert, German Yagyu, Mako Yoshimoto, Kohki |
| author_facet | Robert, German Yagyu, Mako Koizumi, Takaya Naya, Loreto Masclaux‐Daubresse, Céline Yoshimoto, Kohki |
| author_sort | Robert, German |
| collection | INTA Digital |
| 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. |
| format | Artículo |
| id | INTA8757 |
| institution | Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina) |
| language | Inglés |
| publishDate | 2021 |
| publishDateRange | 2021 |
| publishDateSort | 2021 |
| publisher | Wiley |
| publisherStr | Wiley |
| record_format | dspace |
| spelling | INTA87572021-02-26T11:54:07Z Ammonium stress increases microautophagic activity while impairing macroautophagic flux in Arabidopsis roots Robert, German Yagyu, Mako Koizumi, Takaya Naya, Loreto Masclaux‐Daubresse, Céline Yoshimoto, Kohki Ammonium Nitrogen Toxicity Vacuoles Stress Arabidopsis Nitrógeno Amoniacal Toxicidad Vacúola Estres NH4-N NH4 CCZ1-MON1 Macroautophagy Microautophagy Autophagosome-to-vacuole Fusion Vacuole Morphology 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 2021-02-26T11:39:46Z 2021-02-26T11:39:46Z 2020-11-22 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 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 eng info:eu-repo/semantics/restrictedAccess application/pdf Wiley The Plant Journal 105 (4) : 1083-1097 (February 2021) |
| spellingShingle | Ammonium Nitrogen Toxicity Vacuoles Stress Arabidopsis Nitrógeno Amoniacal Toxicidad Vacúola Estres NH4-N NH4 CCZ1-MON1 Macroautophagy Microautophagy Autophagosome-to-vacuole Fusion Vacuole Morphology Robert, German Yagyu, Mako Koizumi, Takaya Naya, Loreto Masclaux‐Daubresse, Céline Yoshimoto, Kohki 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 |
| 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_short | 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 |
| 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 |
| 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 |
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