Roles of CAMTA transcription factors and salicylic acid in configuring the low‐temperature transcriptome and freezing tolerance of Arabidopsis

Abstract

Summary: Previous studies in Arabidopsis thaliana established roles for CALMODULIN BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA 3) in the rapid cold induction of CRT/DRE BINDING FACTOR (CBF) genes CBF 1 and CBF 2, and the repression of salicylic acid (SA) biosynthesis at warm temperature. Here we show that CAMTA 1 and CAMTA 2 work in concert with CAMTA 3 at low temperature (4°C) to induce peak transcript levels of CBF 1, CBF 2 and CBF 3 at 2 h, contribute to up‐regulation of approximately 15% of the genes induced at 24 h, most of which fall outside the CBF pathway, and increase plant freezing tolerance. In addition, CAMTA 1, CAMTA 2 and CAMTA 3 function together to inhibit SA biosynthesis at warm temperature (22°C). However, SA levels increase in A rabidopsis plants that are exposed to low temperature for more than 1 week. We show that this chilling‐induced SA biosynthesis proceeds through the isochorismate synthase (ICS) pathway, with cold induction of ICS 1 (which encodes ICS), and two genes encoding transcription factors that positively regulate ICS 1 – CBP 60g and SARD 1 –, paralleling SA accumulation. The three CAMTA proteins effectively repress the accumulation of ICS 1, CBP 60g and SARD 1 transcripts at warm temperature but not at low temperature. This impairment of CAMTA function may involve post‐transcriptional regulation, as CAMTA transcript levels did not decrease at low temperature. Salicylic acid biosynthesis at low temperature did not contribute to freezing tolerance, but had a major role in configuring the transcriptome, including the induction of ‘defense response’ genes, suggesting the possible existence of a pre‐emptive defense strategy programmed by prolonged chilling temperatures.