The Molecular Basis of Temperature Compensation in the Arabidopsis Circadian Clock

Abstract

Circadian clocks maintain robust and accurate timing over a broad range of physiological temperatures, a characteristic termed temperature compensation. In Arabidopsis thaliana, ambient temperature affects the rhythmic accumulation of transcripts encoding the clock components TIMING OF CAB EXPRESSION1 (TOC1), GIGANTEA (GI), and the partially redundant genes CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY). The amplitude and peak levels increase for TOC1 and GI RNA rhythms as the temperature increases (from 17 to 278C), whereas they decrease for LHY. However, as temperatures decrease (from 17 to 128C), CCA1 and LHY RNA rhythms increase in amplitude and peak expression level. At 278C, a dynamic balance between GI and LHY allows temperature compensation in wild-type plants, but circadian function is impaired in lhy and gi mutant plants. However, at 128C, CCA1 has more effect on the buffering mechanism than LHY, as the cca1 and gi mutations impair circadian rhythms more than lhy at the lower temperature. At 178C, GI is apparently dispensable for free-running circadian rhythms, although partial GI function can affect circadian period. Numerical simulations using the interlocking-loop model show that balancing LHY/CCA1 function against GI and other evening-expressed genes can largely account for temperature compensation in wild-type plants and the temperaturespecific phenotypes of gi mutants.

CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL Function Synergistically in the Circadian Clock of Arabidopsis

“…In wild-type plants, heterodimers of CCA1 and LHY could be important for proper feedback inhibition and in single mutants of cca1 and lhy, CCA1 or LHY may form homodimers, which could maintain rhythmic oscillations but cause the feedback inhibition to occur faster and result in a short-period phenotype. This is consistent with the notion that CCA1 and LHY have different biochemical activities (Gould et al, 2006) and they are only partially redundant in the circadian system.…”

“…CCA1 and LHY bind directly to the promoter of TOC1, negatively regulating TOC1 expression, and TOC1 participates in the positive regulation of CCA1 and LHY expression through an unknown mechanism (Alabadí et al, 2001). Other genes, such as LUX ARRHYTHMO, also known as PHYTOCLOCK1, GI-GANTEA (GI), EARLY FLOWERING3 (ELF3), ELF4, TIME FOR COFFEE, and PSEUDORESPONSE REGU-LATOR3/5/7/9 (PRR3/5/7/9), have also been suggested to function in or close to the central oscillator (Doyle et al, 2002;Hazen et al, 2005;Locke et al, 2005;Nakamichi et al, 2005;Edwards et al, 2006;Gould et al, 2006;Ding et al, 2007;McWatters et al, 2007).…”

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

“…The circadian clock and other physiological responses adjust to environmental temperature changes through altered gene expression (25)(26)(27). Expression of the integral clock component GI is elevated by warm temperature (27°C) (28). The activities of PRR7 and PRR9 are required for temperature entrainment of the circadian clock (16), and their expression is induced following ambient temperature increases (see below).…”

Semi-algebraic optimization of temperature compensation in a general switch-type negative feedback model of circadian clocks

“…Although molecular and theoretical explanations for many aspects of circadian oscillators have been developed over the past decade [6], there have been few attempts to describe temperature compensation on a mathematical kinetic basis [26]. For an overview on other or related attempts to explain temperature compensation the reader is referred to the following papers [12,13,[15][16][17][18]27,28]. However, a discussion of these various approaches on how to "balance P" is beyond the scope of this paper.…”