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

  • EMBO J. 2024 Oct 3. doi: 10.1038/s44318-024-00256-5.
Shashank K Pandey  #  1 ,  Jay Prakash Maurya  #  1  2 ,  Bibek Aryal  #  1 ,  Kamil Drynda  #  3 ,  Aswin Nair  1 ,  Pal Miskolczi  1 ,  Rajesh Kumar Singh  1  4 ,  Xiaobin Wang  1  5 ,  Yujiao Ma  1  6 ,  Tatiana de Souza Moraes  7 ,  Emmanuelle M Bayer  7 ,  Etienne Farcot  3 ,  George W Bassel  8 ,  Leah R Band  3  9 ,  Rishikesh P Bhalerao  10
Affiliations
  • 1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 87, Umeå, Sweden.
  • 2. Plant Development and Molecular Biology Lab, Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, 221005, Uttar Pradesh, India.
  • 3. Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham, NG7 2RD, UK.
  • 4. Biotechnology Division, CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, 176061, India.
  • 5. College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang, 310058, P. R. China.
  • 6. Shandong Academy of Grape, Jinan, Shandong, 250100, P. R. China.
  • 7. Laboratoire de Biogenèse Membranaire, UMR5200, CNRS, Université de Bordeaux, Villenave d'Ornon, France.
  • 8. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.
  • 9. Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK.
  • 10. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 87, Umeå, Sweden. [email protected].
  • # Contributed equally.
PMID: 39363036 DOI: 10.1038/s44318-024-00256-5
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.

Keywords
Callose; Dormancy; Gibberellins; Plasmodesmata; Temperature.
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