Novel transcriptional responses to heat revealed by turning up the heat at night

Abstract

Key message The circadian clock controls many molecular activities, impacting experimental interpretation. We quantify the genome-wide effects of time-of-day on the heat-shock response and the effects of “diurnal bias” in stress experiments. Abstract Heat stress has significant adverse effects on plant productivity worldwide. Most experiments examining heat stress are performed during daytime hours, generating a ‘diurnal bias’ in the pathways and regulatory mechanisms identified. Such bias may confound downstream interpretations and limit our understanding of the full response to heat stress. Here we show that the transcriptional and physiological responses to a sudden heat shock in Arabidopsis are profoundly sensitive to the time of day. We observe that plant tolerance and acclimation to heat shock vary throughout the day and are maximal at dusk. Consistently, over 75% of heat-responsive transcripts show a time of day-dependent response, including many previously characterized heat-response genes. This temporal sensitivity implies a complex interaction between time and temperature where daily variations in basal transcription influence thermotolerance. When we examined these transcriptional responses, we uncovered novel night-response genes and cis -regulatory elements, underpinning new aspects of heat stress responses not previously appreciated. Exploiting this temporal variation can be applied to most environmental responses to understand the underlying network wiring. Therefore, we propose that using time as a perturbagen is an approach that will enhance our understanding of plant regulatory networks and responses to environmental stresses. Electronic supplementary material The online version of this article (10.1007/s11103-019-00873-3) contains supplementary material, which is available to authorized users.

Interaction between the Circadian Clock and Regulators of Heat Stress Responses in Plants

“…A similar response has been observed for DREB2B, and overexpression of the rice OsDREB2A and OsDREB2B showed improved plant tolerance to drought, suggesting a conservation of the regulatory mechanisms across plant species [104,105]. Other DREB TFs, designated CBFs, have been shown to be regulated by cold, high ambient temperatures, and heat stress, implicating them as important regulators linking the clock to temperature stress response mechanisms [43,44,50,58].…”

“…Together, warm temperatures impact multiple levels of gene regulation, including alternative splicing, post-translation, and protein abundance [12,34,41,42]. More recently, it has been shown that the impact on the transcript abundance of clock genes following a 1 h exposure to 30 • C differs depending on the time of day [43]. Circadian gating (controlling the magnitude or the occurrence of a response based on time of day) of cold responses for clock and clock-controlled genes have been previously reported [44].…”

“…In Arabidopsis, HSFA2 and HSFA7b are induced by heat stress in the morning (ZT1) and afternoon (ZT6), respectively, and the induction is higher in the afternoon [50]. In contrast, HSFA3 transcript abundance accumulates to higher levels in the afternoon relative to the morning [43,50]. HSFB1, HSFB2a, and HSFB2b are all heat-induced with higher transcript abundance in the afternoon, whereas HSFC1 gene expression is repressed by heat regardless of time of day [50,90].…”

Expansion of the circadian transcriptome inBrassica rapaand genome-wide diversification of paralog expression patterns

“…Gene ontology enrichment processes for the genes in these daytime phased modules included photosynthesis and abiotic stress response (Dataset S3). However, it should be noted that in general, evening phased genes are likely to be greatly understudied because most experiments are performed during the day (45).…”

“…This led us to wonder whether there is any indication that these pattern changes may contribute to new temporal responses to environmental stimuli such as abiotic stress. The gated stress response has been characterized in several plant species including Arabidopsis, poplar, rice and B. rapa (26,(42)(43)(44)(45). If a time-ofday dependent stress responsive gene in Arabidopsis now has two copies in B. rapa with altered expression patterns does this result in an expanded stress response window or does one copy retain stress response while the other loses it?…”