Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity

Abstract

Circadian rhythms are widespread in nature and reflect the activity of an endogenous biological clock. In metazoans, the circadian system includes a central circadian clock in the brain as well as distinct clocks in peripheral tissues such as the retina or liver. Similarly, plants have distinct clocks in different cell layers and tissues. Here, we show that two different circadian clocks, distinguishable by their sensitivity to environmental temperature signals, regulate the transcription of genes that are expressed in the Arabidopsis thaliana cotyledon. One oscillator, which regulates CAB2 expression, responds preferentially to light-dark versus temperature cycles and fails to respond to the temperature step associated with release from stratification. The second oscillator, which regulates CAT3 expression, responds preferentially to temperature versus light-dark cycles and entrains to the release from stratification. Finally, the phase response curves of these two oscillators to cold pulses are distinct. The phase response curve of the oscillator component TOC1 to cold pulses is similar to that of CAB2, indicating that CAB2 is regulated by a TOC1-containing clock. The existence of two clocks, distinguishable on the basis of their sensitivity to temperature, provides an additional means by which plants may integrate both photoperiodic and temperature signals to respond to the changing seasons. T he circadian clock is an endogenous oscillator with an approximate period of 24 hr that can be synchronized, or entrained, to the exact period of daily oscillations in light and temperature (1). This enables an organism to phase its biological activities to the correct time of day. The sleep-wake cycle in humans, activity and eclosion rhythms in flies, and conidiation in Neurospora are rhythmic processes that display distinct phase angles with the environment (2). In the flowering plant Arabidopsis thaliana, the circadian clock phases the peak mRNA abundance of many genes to distinct times of day (3). Furthermore, the phase angle of specific circadian rhythms with the environmental light-dark (LD) cycle controls seasonal behavior such as flowering (4-6).The clock is temperature-compensated, meaning that the pace of the clock is more or less constant across a range of temperatures and fails to exhibit the acceleration with temperature that characterizes typical enzymatic reactions. Nonetheless, temperature serves as an important environmental time cue and entrainment to temperature cycles has been demonstrated in a number of systems (7,8). It is commonly assumed that light is the dominant environmental time cue for circadian clocks, although few studies have systematically compared light and temperature (9-12). In fact, temperature cycles applied antiphase to LD cycles set the phase angle of multiple rhythms, including CO 2 assimilation in Kalanchoë (13), ethylene production in sorghum (14), and conidiation in Neurospora (15).We compared the relative strengths of temperature cycles and LD cycles as determinants of the ph...

Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana

“…The stability of a number of transcripts has been shown to be under circadian control (41), and the stability of others, including CCA1 and LHY, is light regulated (11). The stabilization of CAT3 mRNA in extended dark obscures an underlying rhythm in CAT3 transcription (24,42). Perhaps elevated temperature during the subjective night destabilizes PRMT5 mRNA, preventing the continued accumulation of PRMT5 mRNA at night in the absence of thermocycles.…”

Genetic and physiological bases for phenological responses to current and predicted climates

“…Most probably reflecting this latitudinal trend, many tree species show marked clines in the critical short-day length that induces bud set at both the phenotypic and allelic level, resulting in bud set at earlier calendar dates and longer days in more northern populations (Bohlenius et al 2006;Hall et al 2007;Luquez et al 2008). Within species or genera, chilling cues may become subordinate to photoperiod cues in the timing of bud burst closer to the tropics and/or the temperatures required to fulfil chilling requirements may rise (Borchert et al 2005;Wilkie et al 2008;Colasanti & Coneva 2009 et al 2002), circadian clock period (Michael et al 2003) and day length sensitivity (Balasubramanian et al 2006a; but see Samis et al 2008) have all been identified. Overall developmental rates or response to endogenous cues may also shift with climate.…”

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

“…Because both PRR7 and PRR9 also participate in clock responses to light (17), temperature entrainment and light entrainment appear to share components. However, the relative contributions of light and temperature to entrainment of the Arabidopsis clock are not well understood, except for the possibility of two oscillators capable of distinguishing light and temperature cues (18).…”