Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Naranjo-Arcos, Maria, Srivastava, Moumita, Deligne, Florian, Bhagat, Prakash Kumar, Mansi, Mansi, Sadanandom, Ari, Vert, Grégory
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
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
_version_ 1784891582547230720
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
work_keys_str_mv AT naranjoarcosmaria sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT srivastavamoumita sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT deligneflorian sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT bhagatprakashkumar sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT mansimansi sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT sadanandomari sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature
AT vertgregory sumodesumoylationofthebri1brassinosteroidreceptormodulatesplantgrowthresponsestotemperature