A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis

Plant Cell. 2012 Jun;24(6):2427-42. doi: 10.1105/tpc.112.098723. Epub 2012 Jun 19.

Abstract

The circadian clock synchronizes biological processes to daily cycles of light and temperature. Clock components, including CIRCADIAN CLOCK-ASSOCIATED1 (CCA1), are also associated with cold acclimation. However, it is unknown how CCA1 activity is modulated in coordinating circadian rhythms and cold acclimation. Here, we report that self-regulation of Arabidopsis thaliana CCA1 activity by a splice variant, CCA1β, links the clock to cold acclimation. CCA1β interferes with the formation of CCA1α-CCA1α and LATE ELONGATED HYPOCOTYL (LHY)-LHY homodimers, as well as CCA1α-LHY heterodimers, by forming nonfunctional heterodimers with reduced DNA binding affinity. Accordingly, the periods of circadian rhythms were shortened in CCA1β-overexpressing transgenic plants (35S:CCA1β), as observed in the cca1 lhy double mutant. In addition, the elongated hypocotyl and leaf petiole phenotypes of CCA1α-overexpressing transgenic plants (35S:CCA1α) were repressed by CCA1β coexpression. Notably, low temperatures suppressed CCA1 alternative splicing and thus reduced CCA1β production. Consequently, whereas the 35S:CCA1α transgenic plants exhibited enhanced freezing tolerance, the 35S:CCA1β transgenic plants were sensitive to freezing, indicating that cold regulation of CCA1 alternative splicing contributes to freezing tolerance. On the basis of these findings, we propose that dynamic self-regulation of CCA1 underlies the clock regulation of temperature responses in Arabidopsis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism*
  • Circadian Clocks*
  • Cold Temperature
  • DNA, Plant / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Gene Expression Regulation, Plant*
  • Plants, Genetically Modified
  • Protein Isoforms
  • Protein Multimerization
  • Stress, Physiological
  • Temperature
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism*

Substances

  • Arabidopsis Proteins
  • CCA1 protein, Arabidopsis
  • DNA, Plant
  • DNA-Binding Proteins
  • LHY protein, Arabidopsis
  • Protein Isoforms
  • Transcription Factors