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

Abstract

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.

Citation

Naranjo-Arcos, M., Srivastava, M., Deligne, F., Bhagat, P. K., Mansi, M., Sadanandom, A., & Vert, G. (2023). SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature. Proceedings of the National Academy of Sciences, 120(4), Article 2217255120. https://doi.org/10.1073/pnas.2217255120

• Journal Article Type: Article
• Acceptance Date: Dec 16, 2022
• Online Publication Date: Jan 18, 2023
• Publication Date: Jan 24, 2023
• Deposit Date: Jan 23, 2024
• Publicly Available Date: Jan 23, 2024
• Journal: Proceedings of the National Academy of Sciences
• Print ISSN: 0027-8424
• Electronic ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Peer Reviewed: Peer Reviewed
• Volume: 120
• Issue: 4
• Article Number: 2217255120
• DOI: https://doi.org/10.1073/pnas.2217255120
• Public URL: https://durham-repository.worktribe.com/output/2161933