A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release

Pandey, Shashank K; Maurya, Jay Prakash; Aryal, Bibek; Drynda, Kamil; Nair, Aswin; Miskolczi, Pal; Singh, Rajesh Kumar; Wang, Xiaobin; Ma, Yujiao; de Souza Moraes, Tatiana; Bayer, Emmanuelle M; Farcot, Etienne; Bassel, George W; Band, Leah R; Bhalerao, Rishikesh P

Abstract

The control of cell–cell communication via plasmodesmata (PD) plays a key role in plant development. In tree buds, low-temperature conditions (LT) induce a switch in plasmodesmata from a closed to an open state, which restores cell-to-cell communication in the shoot apex and releases dormancy. Using genetic and cell-biological approaches, we have identified a previously uncharacterized transcription factor, Low-temperature-Induced MADS-box 1 (LIM1), as an LT-induced, direct upstream activator of the gibberellic acid (GA) pathway. The LIM1-GA module mediates low temperature-induced plasmodesmata opening, by negatively regulating callose accumulation to promote dormancy release. LIM1 also activates expression of FT1 (FLOWERING LOCUS T), another LT-induced factor, with LIM1-FT1 forming a coherent feedforward loop converging on low-temperature regulation of gibberellin signaling in dormancy release. Mathematical modeling and experimental validation suggest that negative feedback regulation of LIM1 by gibberellin could play a crucial role in maintaining the robust temporal regulation of bud responses to low temperature. These results reveal genetic factors linking temperature control of cell–cell communication with regulation of seasonally-aligned growth crucial for adaptation of trees.

Citation

Pandey, S. K., Maurya, J. P., Aryal, B., Drynda, K., Nair, A., Miskolczi, P., Singh, R. K., Wang, X., Ma, Y., de Souza Moraes, T., Bayer, E. M., Farcot, E., Bassel, G. W., Band, L. R., & Bhalerao, R. P. (2024). A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release. EMBO Journal, 43(23), 5793-5812. https://doi.org/10.1038/s44318-024-00256-5

• Journal Article Type: Article
• Acceptance Date: Sep 12, 2024
• Online Publication Date: Oct 3, 2024
• Publication Date: Dec 2, 2024
• Deposit Date: Nov 28, 2024
• Publicly Available Date: Nov 28, 2024
• Journal: EMBO Journal
• Print ISSN: 0261-4189
• Electronic ISSN: 1460-2075
• Publisher: EMBO Press
• Peer Reviewed: Peer Reviewed
• Volume: 43
• Issue: 23
• Pages: 5793-5812
• DOI: https://doi.org/10.1038/s44318-024-00256-5
• Keywords: Plasmodesmata, Callose, Gibberellins, Temperature, Dormancy
• Public URL: https://nottingham-repository.worktribe.com/output/40589778
• Publisher URL: https://www.embopress.org/doi/full/10.1038/s44318-024-00256-5