Model selection reveals control of cold signalling by evening‐phased components of the plant circadian clock

Abstract

Circadian clocks confer advantages by restricting biological processes to certain times of day through the control of specific phased outputs. Control of temperature signalling is an important function of the plant oscillator, but the architecture of the gene network controlling cold signalling by the clock is not well understood. Here we use a model ensemble fitted to time-series data and a corrected Akaike Information Criterion (AICc) analysis to extend a dynamic model to include the control of the key cold-regulated transcription factors C-REPEAT BINDING FACTORs 1–3 (CBF1, CBF2, CBF3). AICc was combined with in silico analysis of genetic perturbations in the model ensemble, and selected a model that predicted mutant phenotypes and connections between evening-phased circadian clock components and CBF3 transcriptional control, but these connections were not shared by CBF1 and CBF2. In addition, our model predicted the correct gating of CBF transcription by cold only when the cold signal originated from the clock mechanism itself, suggesting that the clock has an important role in temperature signal transduction. Our data shows that model selection could be a useful method for the expansion of gene network models.

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

“…The circadian clock is also involved in the cold response because the EE (AATATC) is a conserved motif in the promoter of cold-inducible genes (Mikkelsen and Thomashow, 2009;Maruyama et al, 2012). PRR5, PRR7, PRR9, and TOC1 were also reported to be involved in freezing tolerance (Nakamichi et al, 2009;Keily et al, 2013). Our results indicate that COR27 and COR28 work redundantly to regulate period length in the circadian clock ( Figure 6) and suggest that COR27 and COR28 balance flowering and freezing tolerance via circadian clock regulation.…”

“…The prr5-10 prr7-10 prr9-11 triple mutant showed increased CBF expression and increased freezing tolerance (Nakamichi et al, 2009). Similarly, the toc1-101 mutant also showed increased expression of CBF3 and increased freezing tolerance (Keily et al, 2013). Cold may also affect the clock function, as it is reported that CBF1 binds directly to the LUX promoter to regulate the transcription of LUX (Chow et al, 2014).…”

Transcriptional Regulation of LUX by CBF1 Mediates Cold Input to the Circadian Clock in Arabidopsis

“…Loss of CCA1/LHY impairs freezing tolerance [30–32] while CCA1 overexpression promotes freezing tolerance [33]. In addition, mutation of PRR9/7/5 and TOC1 enhances freezing tolerance, and PRR5, PRR7, and TOC1 associate with CBF promoters [9,34–37]. While the mechanism is unknown, loss of GIGANTEA ( GI ) also causes freezing sensitivity but independently of changes in CBF expression [38].…”

“…This demonstrates that LUX contributes to freezing tolerance. Recently the lux-2 mutant was reported to have similar sensitivity as wildtype to freezing stress in the absence of cold-acclimation [37]. Since the lux-1 , lux-2 , and lux-4 mutations all cause premature stop codons and affect clock processes similarly [1], this suggests LUX may have a very specific role during the acclimation process.…”

Mathematical Models Light Up Plant Signaling

“…Examples of circadian-regulated processes that affect plant growth include hypocotyl elongation, opening of stomata, cold acclimation, photosynthetic rate, hormone signaling, and starch turnover (Dodd et al, 2005;Harmer et al, 2000;Nozue et al, 2007;Legnaioli et al, 2009;Graf et al, 2010;Dong et al, 2011;Nomoto et al, 2012;Keily et al, 2013). Here, we look at how the circadian clock enables plants to perceive daylength, such that they flower and reproduce in favorable seasonal conditions.…”