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

Authors: THINES, BRIAN - University Of California; Harmon, Frank

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/30/2010
Publication Date: 2/16/2010
Citation: Thines, B., Harmon, F.G. 2010. Ambient temperature response establishes ELF3 as a required component of the Arabidopsis core circadian clock. Proceedings of the National Academy of Sciences. 107(7):3257-3262.

Interpretive Summary: All higher plants possess endogenous circadian clocks to synchronize internal physiological processes with environmental cycles to optimize timing of biological events on daily and seasonal timescales. To ensure correct synchronization, plants perceive external light and temperature cues that they use to adjust the endogenous oscillator to match local environmental conditions. This work shows the long known circadian clock-associated protein EARLY FLOWERING 3 (ELF3) is required for the model plant Arabidopsis to produce circadian rhythms under all conditions, which is a novel functional assignment. Furthermore, plants that could not generate endogenous rhythms, like the elf3 mutant, were unable to properly respond to temperature changes; instead, the mutant plants behaved as if temperature signals were always present. Therefore, the rhythms of the circadian clock are necessary for plants to accurately respond and set their circadian clocks to temperature cues. Plants with circadian clock mutations causing rhythms to be out of sync with environmental cycles have reduced fitness. From a crop plant perspective, optimizing circadian clock performance to elevate fitness is an unexamined area that hold promise to increase crop yield.

Technical Abstract: Circadian clocks synchronize internal processes with environmental cycles to ensure optimal timing of biological events on daily and seasonal timescales. 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 dark-grown, or etiolated, null elf3-1 seedlings, with the clock entrained by thermocycles, to evaluate the light-dependent nature of the elf3 mutant phenotype. Circadian rhythms were absent from etiolated elf3-1 seedlings after exposure to temperature cycles and this mutant failed to exhibit classical 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 induction of temperature-responsive genes in elf3-1. In fact, warm temperature-responsive genes remained in a constitutively “ON” state due to 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 and, taken together, support a model 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.