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

Sammanfattning

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.Every year, deciduous trees use the cold of winter to prime their buds for opening in the spring; however, the mechanism of this priming has remained obscure. The current work identifies signals that open plasmodesmata and allow dormancy-release messages to enter the bud.The MADS-box transcription factor LIM1 promotes low temperature induced bud dormancy release.LIM1 is a negative regulator of callose accumulation and facilitates the opening of plasmodesmata.LIM1 acts upstream of the florigen component FT1 and the gibberellin biosynthesis pathway in dormancy release.LIM1 is a transcription factor that opens plasmodesmata and allows bud break.

Nyckelord

Dormancy; Temperature; Plasmodesmata; Callose; Gibberellins

Publicerad i

EMBO Journal
2024, volym: 43, nummer: 23, sidor: 5793-5812
Utgivare: SPRINGERNATURE

SLU författare

• Pandey, Shashank

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    

• Prakash, Jay

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    
  • Banaras Hindu University

• Aryal, Bibek

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    

• Nair, Aswin

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    

• Miskolczi, Pal Csaba

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    

• Singh, Rajesh

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    
  • Council of Scientific and Industrial Research (CSIR)

• Wang, Xiaobin

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    
  • Zhejiang University

• Yujiao, Ma

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    
  • Shandong Agricultural University

• Bhalerao, Rishikesh P.

  • Institutionen för skoglig genetik och växtfysiologi, Sveriges lantbruksuniversitet
    

UKÄ forskningsämne

Cellbiologi

Publikationens identifierare

• DOI: https://doi.org/10.1038/s44318-024-00256-5

Permanent länk till denna sida (URI)

https://res.slu.se/id/publ/132904