Disruption of the Arabidopsis Circadian Clock Is Responsible for Extensive Variation in the Cold-Responsive Transcriptome      

Abstract

In plants, low temperature causes massive transcriptional changes, many of which are presumed to be involved in the process of cold acclimation. Given the diversity of developmental and environmental factors between experiments, it is surprising that their influence on the identification of cold-responsive genes is largely unknown. A systematic investigation of genes responding to 1 d of cold treatment revealed that diurnal-and circadian-regulated genes are responsible for the majority of the substantial variation between experiments. This is contrary to the widespread assumption that these effects are eliminated using paired diurnal controls. To identify the molecular basis for this variation, we performed targeted expression analyses of diurnal and circadian time courses in Arabidopsis (Arabidopsis thaliana). We show that, after a short initial cold response, in diurnal conditions cold reduces the amplitude of cycles for clock components and dampens or disrupts the cycles of output genes, while in continuous light all cycles become arrhythmic. This means that genes identified as cold-responsive are dependent on the time of day the experiment was performed and that a control at normal temperature will not correct for this effect, as was postulated up to now. Time of day also affects the number and strength of expression changes for a large number of transcription factors, and this likely further contributes to experimental differences. This reveals that interactions between cold and diurnal regulation are major factors in shaping the cold-responsive transcriptome and thus will be an important consideration in future experiments to dissect transcriptional regulatory networks controlling cold acclimation. In addition, our data revealed differential effects of cold on circadian output genes and a unique regulation of an oscillator component, suggesting that cold treatment could also be an important tool to probe circadian and diurnal regulatory mechanisms.

Global analysis of gene expression in maize leaves treated with low temperature. II. Combined effect of severe cold (8 °C) and circadian rhythm

“…Indeed, we found disruption of the expression patterns of these clock genes in maize by severe cold. Some of them lost their pronounced temporal profile and instead were expressed at a nearly constant level (TOC1, GI, PRR5, PRR7 and PRR9), similarly as has been observed in A. thaliana at 4 °C (Bieniawska et al 2008); other clock genes, however, responded in a markedly different manner by undergoing a gradual increase (LHY/CCA1, RVE2) or decrease (LUX) of expression, suggesting in all four cases a temporal shift of the transcript extremum by ca. 3 h. This response was not unique to the CM109 line studied here.…”

“…A major factor affecting all aspects of plant physiology is the photoperiod, but only recently has it been fully recognized that studies of plant stress responses should not neglect rhythmic gene expression driven by the circadian clock (Bieniawska et al 2008). Some studies on the Arabidopsis thaliana response to cold have accommodated this fact already (Bieniawska et al 2008;Espinoza et al 2010).…”

“…Some studies on the Arabidopsis thaliana response to cold have accommodated this fact already (Bieniawska et al 2008;Espinoza et al 2010). Notably, expression of C-REPEAT BINDING FAC-TORS (CBFs) involved in the cold signaling in A. thaliana (Huang et al 2012) has been shown to be regulated by core clock components CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) through the CCA1-Binding Site (CBS) and EVENING ELE-MENT (EE) regulatory elements in their promoters (Fowler 2005;Dong et al 2011).…”

Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock

“…How CRYs, phytochromes, and UVR8 transduce light signals to the clock is largely unknown. Cold also acts as a clock input, as transcription of clock genes is damped at 4°C (Bieniawska et al, 2008), and low temperature-associated alternative splicing of CCA1 mediates clock responses to low temperatures. The lowtemperature signal is transduced into the clock by the CCA1b isoform, whereas freezing tolerance is enhanced by the CCA1a isoform (Seo et al, 2012).…”

Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock

“…The circadian clock and other physiological responses adjust to environmental temperature changes through altered gene expression (25)(26)(27). Expression of the integral clock component GI is elevated by warm temperature (27°C) (28).…”