The temperature sensor TWA1 is required for thermotolerance in Arabidopsis

Nature. 2024 May;629(8014):1126-1132. doi: 10.1038/s41586-024-07424-x. Epub 2024 May 15.

Abstract

Plants exposed to incidences of excessive temperatures activate heat-stress responses to cope with the physiological challenge and stimulate long-term acclimation1,2. The mechanism that senses cellular temperature for inducing thermotolerance is still unclear3. Here we show that TWA1 is a temperature-sensing transcriptional co-regulator that is needed for basal and acquired thermotolerance in Arabidopsis thaliana. At elevated temperatures, TWA1 changes its conformation and allows physical interaction with JASMONATE-ASSOCIATED MYC-LIKE (JAM) transcription factors and TOPLESS (TPL) and TOPLESS-RELATED (TPR) proteins for repressor complex assembly. TWA1 is a predicted intrinsically disordered protein that has a key thermosensory role functioning through an amino-terminal highly variable region. At elevated temperatures, TWA1 accumulates in nuclear subdomains, and physical interactions with JAM2 and TPL appear to be restricted to these nuclear subdomains. The transcriptional upregulation of the heat shock transcription factor A2 (HSFA2) and heat shock proteins depended on TWA1, and TWA1 orthologues provided different temperature thresholds, consistent with the sensor function in early signalling of heat stress. The identification of the plant thermosensors offers a molecular tool for adjusting thermal acclimation responses of crops by breeding and biotechnology, and a sensitive temperature switch for thermogenetics.

MeSH terms

  • Arabidopsis Proteins* / chemistry
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Arabidopsis* / physiology
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Nucleus / metabolism
  • Gene Expression Regulation, Plant
  • Heat Shock Transcription Factors / genetics
  • Heat Shock Transcription Factors / metabolism
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Intrinsically Disordered Proteins* / chemistry
  • Intrinsically Disordered Proteins* / metabolism
  • Nuclear Pore Complex Proteins / metabolism
  • Repressor Proteins / metabolism
  • Signal Transduction
  • Temperature*
  • Thermosensing* / genetics
  • Thermosensing* / physiology
  • Thermotolerance* / genetics
  • Thermotolerance* / physiology
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • Heat Shock Transcription Factors
  • Heat-Shock Proteins
  • HSFA2 protein, Arabidopsis
  • Intrinsically Disordered Proteins
  • JAM2 protein, Arabidopsis
  • Nuclear Pore Complex Proteins
  • Repressor Proteins
  • topless protein, Arabidopsis
  • TPR protein, Arabidopsis
  • Transcription Factors