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SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature
Brassinosteroids (BRs) are a class of steroid molecules perceived at the cell surface that act as plant hormones. The BR receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) offers a model to understand receptor-mediated signaling in plants and the role of post-translational modifications. Here we identify...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942830/ https://www.ncbi.nlm.nih.gov/pubmed/36652487 http://dx.doi.org/10.1073/pnas.2217255120 |
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author | Naranjo-Arcos, Maria Srivastava, Moumita Deligne, Florian Bhagat, Prakash Kumar Mansi, Mansi Sadanandom, Ari Vert, Grégory |
author_facet | Naranjo-Arcos, Maria Srivastava, Moumita Deligne, Florian Bhagat, Prakash Kumar Mansi, Mansi Sadanandom, Ari Vert, Grégory |
author_sort | Naranjo-Arcos, Maria |
collection | PubMed |
description | Brassinosteroids (BRs) are a class of steroid molecules perceived at the cell surface that act as plant hormones. The BR receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) offers a model to understand receptor-mediated signaling in plants and the role of post-translational modifications. Here we identify SUMOylation as a new modification targeting BRI1 to regulate its activity. BRI1 is SUMOylated in planta on two lysine residues, and the levels of BRI1 SUMO conjugates are controlled by the Desi3a SUMO protease. Loss of Desi3a leads to hypersensitivity to BRs, indicating that Desi3a acts as a negative regulator of BR signaling. Besides, we demonstrate that BRI1 is deSUMOylated at elevated temperature by Desi3a, leading to increased BRI1 interaction with the negative regulator of BR signaling BIK1 and to enhanced BRI1 endocytosis. Loss of Desi3a or BIK1 results in increased response to temperature elevation, indicating that BRI1 deSUMOylation acts as a safety mechanism necessary to keep temperature responses in check. Altogether, our work establishes BRI1 deSUMOylation as a molecular crosstalk mechanism between temperature and BR signaling, allowing plants to translate environmental inputs into growth response. |
format | Online Article Text |
id | pubmed-9942830 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-99428302023-07-18 SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature Naranjo-Arcos, Maria Srivastava, Moumita Deligne, Florian Bhagat, Prakash Kumar Mansi, Mansi Sadanandom, Ari Vert, Grégory Proc Natl Acad Sci U S A Biological Sciences Brassinosteroids (BRs) are a class of steroid molecules perceived at the cell surface that act as plant hormones. The BR receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) offers a model to understand receptor-mediated signaling in plants and the role of post-translational modifications. Here we identify SUMOylation as a new modification targeting BRI1 to regulate its activity. BRI1 is SUMOylated in planta on two lysine residues, and the levels of BRI1 SUMO conjugates are controlled by the Desi3a SUMO protease. Loss of Desi3a leads to hypersensitivity to BRs, indicating that Desi3a acts as a negative regulator of BR signaling. Besides, we demonstrate that BRI1 is deSUMOylated at elevated temperature by Desi3a, leading to increased BRI1 interaction with the negative regulator of BR signaling BIK1 and to enhanced BRI1 endocytosis. Loss of Desi3a or BIK1 results in increased response to temperature elevation, indicating that BRI1 deSUMOylation acts as a safety mechanism necessary to keep temperature responses in check. Altogether, our work establishes BRI1 deSUMOylation as a molecular crosstalk mechanism between temperature and BR signaling, allowing plants to translate environmental inputs into growth response. National Academy of Sciences 2023-01-18 2023-01-24 /pmc/articles/PMC9942830/ /pubmed/36652487 http://dx.doi.org/10.1073/pnas.2217255120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Naranjo-Arcos, Maria Srivastava, Moumita Deligne, Florian Bhagat, Prakash Kumar Mansi, Mansi Sadanandom, Ari Vert, Grégory SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title | SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title_full | SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title_fullStr | SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title_full_unstemmed | SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title_short | SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature |
title_sort | sumo/desumoylation of the bri1 brassinosteroid receptor modulates plant growth responses to temperature |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942830/ https://www.ncbi.nlm.nih.gov/pubmed/36652487 http://dx.doi.org/10.1073/pnas.2217255120 |
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