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

Abstract

Circadian clocks synchronize internal processes with environmental cycles to ensure optimal timing of biological events on daily and seasonal time scales. External light and temperature cues set the core molecular oscillator to local conditions. In Arabidopsis, EARLY FLOWERING 3 (ELF3) is thought to act as an evening-specific repressor of light signals to the clock, thus serving a zeitnehmer function. Circadian rhythms were examined in completely darkgrown, or etiolated, null elf3-1 seedlings, with the clock entrained by thermocycles, to evaluate whether the elf3 mutant phenotype was light-dependent. Circadian rhythms were absent from etiolated elf3-1 seedlings after exposure to temperature cycles, and this mutant failed to exhibit classic indicators of entrainment by temperature cues, consistent with global clock dysfunction or strong perturbation of temperature signaling in this background. Warm temperature pulses failed to elicit acute induction of temperatureresponsive genes in elf3-1. In fact, warm temperature-responsive genes remained in a constitutively "ON" state because of clock dysfunction and, therefore, were insensitive to temperature signals in the normal time of day-specific manner. These results show ELF3 is broadly required for circadian clock function regardless of light conditions, where ELF3 activity is needed by the core oscillator to allow progression from day to night during either light or temperature entrainment. Furthermore, robust circadian rhythms appear to be a prerequisite for etiolated seedlings to respond correctly to temperature signals.temperature signaling | temperature entrainment | luciferase | circadian rhythms | transcription T he rotation of Planet Earth creates predictable daily environmental fluctuations of light and dark along with concomitant oscillations in temperature. The circadian clock is an endogenous timekeeper that anticipates these predictable changes in the environment, confers rhythmic behavior to biological processes, and optimally phases biological activities to specific times of the day. Circadian clocks are widespread in nature, and processes under their control range from sleep-wake cycles in humans to daily expression of photosynthetic genes in plants. Clocks also time seasonal responses, such as the flowering transition in many plant species.Core molecular oscillators in eukaryotes incorporate interlocked transcription-translation feedback loops. In the model plant Arabidopsis thaliana, three such loops are critical to generation and maintenance of circadian rhythms. The loop first discovered is composed of the pseudoresponse regulator TOC1 (1) and two partially redundant Myb-like transcription factors, CCA1 (2) and LHY (3). Morning expression of CCA1 and LHY represses TOC1 expression by binding to its promoter (4), and circadian accumulation of TOC1 in the evening helps to induce CCA1 and LHY. A second morning-phased loop includes two TOC1-related proteins, PRR7 and PRR9 (5, 6). CCA1 and LHY induce PRR7 and PRR9 expression, whereas the two PRRs subseq...

HsfB2b-mediated repression ofPRR7directs abiotic stress responses of the circadian clock

“…We tested the resetting behavior of CCA1:LUC to heat pulses (38°C) applied in LL after entrainment to 12-h light:12-h dark (12L:12D) cycles and constant 22°C. In agreement with an earlier report (29), Col-0 seedlings displayed phase delays from subjective late day to middle of the night, and advances from late night to late morning (i.e., exhibiting little resetting during the day). Under these conditions, HsfB2b-ox displayed no phase advances compared with Col-0, along with a later breakpoint (Fig.…”

“…To test the effect of heat as an entrainment signal, we performed a temperature phase response curve (tPRC). We note that the shape of the warm tPRC (transfer from 18°C to 22°C) is similar to the cold tPRC (transfer from 22°C to 12°C); however, the break point (switch from phase delays to advances) is ∼CT6 (circadian time, CT) for the cold tPRC and ∼CT18 for warm tPRC (28,29). We tested the resetting behavior of CCA1:LUC to heat pulses (38°C) applied in LL after entrainment to 12-h light:12-h dark (12L:12D) cycles and constant 22°C.…”

Jumonji domain protein JMJD5 functions in both the plant and human circadian systems

“…We therefore obtained microarray expression data generated from 79 different Arabidopsis samples (representing a wide variety of developmental stages and diverse organs) (20) and calculated the Pearson correlation coefficients between TOC1 and each gene on the ATH1 array. The gene most highly correlated with TOC1 (r = 0.77) was EARLY FLOWERING 3 (ELF3; Table S1), a gene involved both in light input to the clock and in central clock function (21)(22)(23), thereby validating our approach. Because genes involved in the circadian clock are themselves frequently expressed with a circadian oscillation (3, 13), we examined the daily patterns of expression of our candidate genes using previously published microarray data (2).…”

“…Intriguingly, JMJD5 shares these differential effects on clock gene expression with LUX ARRHYTHMO (LUX), ELF3, and ELF4, which are all evening-phased genes that have yet to be ascribed specific positions within the circadian circuitry (21,23,38,39). Like JMJD5, loss of ELF3, ELF4, or LUX causes decreased expression of CCA1 and LHY without strongly affecting TOC1 expression levels (38,(40)(41)(42).…”

Heat Stress Responses and Thermotolerance

“…Temperature variations play a role in the reset of internal clocks and diurnal synchronization [7]. For certain species, exposure to a low temperature is necessary to trigger developmental processes such as flowering [8] or germination [9].…”