Genome-wide circadian gating of a cold temperature response in bread wheat

Abstract

Circadian rhythms coordinate the responses of organisms to their daily fluctuating environments, by establishing a temporal program of gene expression. This schedules aspects of metabolism, physiology, development and behaviour according to the time of day. Circadian regulation in plants is extremely pervasive, and is important because it underpins both productivity and seasonal reproduction. Circadian regulation extends to control of environmental responses through a regulatory mechanism known as circadian gating, whereby the circadian clock regulates the response to environmental cues such that the magnitude of response varies according to the time of day. Here, we show that there is genome-wide circadian gating of responses to cold temperatures in plants. By using bread wheat as an experimental model, we establish that circadian gating is crucial to the programs of gene expression that underlie the environmental responses of a crop of major socioeconomic importance. Furthermore, we identify that circadian gating of cold temperature responses are distributed unevenly across the three wheat subgenomes, which might reflect the geographical origins of the ancestors of modern wheat.

Low-temperature and circadian signals are integrated by the sigma factor SIG5

“…3a). The different sets of cold-responsive transcripts at the two time points are consistent with the notion that there is circadian gating of the cold-responsive transcriptome in plants 47 . We compared our cold-responsive transcript set in Col-0 with that of Zhao et al (3 h cold treatment) 48 and found that 42.5% (ZT29) and 13.4% (ZT45) of cold-responsive transcripts were shared between the studies (Extended Data Fig.…”

Time of day and genotype sensitivity adjust molecular responses to temperature stress in sorghum

“…In sorghum, similar proportions (25-34%) of the heat-responsive transcriptome are gated by the time of day, depending on the genotype (Figure 2C). The genome-wide gating response to temperature is not restricted to heat stress and was also observed under cold stress, as previously reported in Arabidopsis (Blair et al 2019), and recently in wheat (Graham et al 2022).…”

“…In terms of heat stress, the response for Sb_GI is similar to what was observed in Arabidopsis where the increased transcript accumulation occurs before (morning) and after (subjective dark) the peak of GI's expression . In a recent study in wheat, TaPRR73 and TaGI are also the two oscillator components that show strong perturbation in response to cold stress resulting in a delay in their peak of expression (Graham et al 2022). These observations suggest that the sensitivity to temperature for some oscillator components may be conserved across species while others may not be.…”

“…Alternatively, different circadian signaling components may separately regulate expression rhythmicity under control conditions and gate stress responsiveness depending on the plant as suggested by Graham et al (2022) for cold responses in wheat.…”

“…In rice panicles, rhythmic transcripts were observed to be more sensitive to warm nighttime temperatures than those that were nonrhythmic (Desai et al 2021). Furthermore, more recent work showed that in bread wheat the transcriptome response to cold stress is gated, with variations across the three wheat sub-genomes (Graham, Paajanen, Edwards & Dodd 2022). Together suggesting that time of day or gating of temperature stress responses play key roles in the physiological outputs of important crop species.…”