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First published online April 14, 2006; 10.1105/tpc.105.039990

The Plant Cell 18:1177-1187 (2006)
© 2006 American Society of Plant Biologists

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The Molecular Basis of Temperature Compensation in the Arabidopsis Circadian Clock[W]

Peter D. Goulda, James C.W. Lockeb,c,d, Camille Laruea, Megan M. Southernc, Seth J. Davise, Shigeru Hananoe, Richard Moylef,g, Raechel Milichf, Joanna Putterillf, Andrew J. Millard,h,1 and Anthony Halla,1

a School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, United Kingdom
b Department of Physics, University of Warwick, Coventry CV4 7AL, United Kingdom
c Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
d Interdisciplinary Programme for Cellular Regulation, University of Warwick, Coventry CV4 7AL, United Kingdom
e Max Planck Institute for Plant Breeding, Cologne D-50829, Germany
f University of Auckland, School of Biological Sciences, Private Bag 92019, Auckland, New Zealand
g Botany Department, School of Integrative Biology, University of Queensland, Brisbane Qld 4072, Australia
h Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3JH, United Kingdom

1 To whom correspondence should be addressed. E-mail andrew.millar{at}ed.ac.uk or anthony.hall{at}liverpool.ac.uk; fax 44-0131-6505392 or 44-0151-7954403.

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 27°C), whereas they decrease for LHY. However, as temperatures decrease (from 17 to 12°C), CCA1 and LHY RNA rhythms increase in amplitude and peak expression level. At 27°C, 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 12°C, 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 17°C, 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 temperature-specific phenotypes of gi mutants.


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