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© 2005 American Society of Plant Biologists
Temperature Entrainment of the Arabidopsis Circadian Clockneckardt{at}aspb.org
Most eukaryotic organisms as well as some prokaryotes (cyanobacteria) have an endogenous circadian clock that keeps track of the earth's 24-h day/night cycle and regulates the activity of numerous metabolic pathways. The existence of the circadian clock as an endogenous feature of organisms and not merely a response to the presence or absence of sunlight was recognized in plants as early as the 18th and 19th centuries. It had been known since ancient times that certain plants, notably the sensitive plant Mimosa pudica, fold their leaves shut at night and open them during the day. The French astronomer Jean de Mairan in 1729, and botanists Henri-Louis Duhamel and Augustin de Candolle in 1758 and 1832, respectively, were motivated to ask if this was an innate property of the plant as opposed to a passive response and conducted the simple experiments of observing plants maintained in constant darkness or constant light. Their observations that plants in constant conditions continued to open and shut their leaves at the appropriate times suggested the existence of an endogenous circadian clock. De Candolle showed that the period of leaf opening and folding in Mimosa plants was 22 h under constant light, demonstrating the free-running nature of circadian clocks (Coleman, 1986
There are three hallmarks of circadian clock–controlled rhythms: (1) they are free running and will continue to oscillate with an approximate 24-h period in the absence of external stimuli, (2) they are entrainable by external stimuli, such as light and temperature, and (3) in contrast with most metabolic processes that are strongly affected by changes in temperature, overall periodicity is unaffected by temperature (McClung et al., 2002
In all organisms studied, including plants (Arabidopsis), fungi (Neurospora), mammals (mainly rodents, and to some extent humans), and insects (Drosophila), the central oscillator consists of a complex feedback loop, or multiple interwoven loops, involving both positive and negative regulation, essential features of which include posttranslational protein modifications that precisely control degradation and shuttling of principal factors between the nucleus and cytoplasm.
The mammalian circadian clock is a complex system composed of numerous tissue-specific clocks, all regulated by a master pacemaker that resides in the suprachiasmatic nuclei in the brain (reviewed in Albrecht and Eichele, 2003
The clockwork mechanism in higher plants also consists of positive and negative feedback loops, which in Arabidopsis involve the single-Myb domain transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE AND ELONGATED HYPOCOTYL (LHY) and the pseudoresponse regulator protein TIMING OF CAB EXPRESSION 1/PSEUDO-RESPONSE REGULATOR 1 (TOC1/PRR1) (Alabadí et al., 2001  ). CCA1 and LHY inhibit TOC1 transcription, whereas TOC1 directly or indirectly promotes transcription of CCA1 and LHY (see figure). The loops are regulated by turnover of CCA1 and LHY via an unidentified mechanism and of TOC1 by proteasomal degradation mediated by the F-box protein ZEITLUPE (ZTL; Más et al., 2003a; Han et al., 2004).
In addition to TOC1/PRR1, the transcription of four other Arabidopsis PRR genes (PRR3, 5, 7, and 9) oscillates with a circadian period. Matsushika et al. (2000)
Circadian clocks are continually entrained by environmental factors, notably light and temperature, which act continually to reset the clock mechanism and thus synchronize output rhythms with changes in daylight hours during the year. Light is the most powerful and best-characterized entrainment signal in plants. The phytochrome (PHYA-PHYE) and cryptochrome (CRY1 and CRY2) photoreceptors in Arabidopsis have all been shown to function in light entrainment of the clock (reviewed in Devlin and Kay, 2001 ). ZTL is an interesting multidomain protein that appears to play critical roles both in the regulation of core clock proteins and in light entrainment of the clock. In addition to the F-box domain, which is presumed to function in targeting of interacting partners (such as TOC1) for proteasomal degradation, ZTL contains a LOV domain similar to that of PHOT1 and other phototropins, suggesting that it may function as a photoreceptor, and KELCH repeats, which are known to be involved in protein–protein interactions in numerous other proteins. ZTL has been shown to interact with the PHYB and CRY1 photoreceptors in a yeast two-hybrid system (Jarillo et al., 2001), so it is suggested that ZTL may function in light entrainment of the clock. Although circadian clocks are temperature compensated, which means that overall clock period is constant over a range of temperatures, temperature changes can act to entrain or reset the clock output patterns. However, very little is known about the mechanism of temperature entrainment. In this issue of The Plant Cell, Salomé and McClung (pages 791–803) analyze prr7 and prr9 single and double mutants and show that PRR7 and PRR9 have overlapping functions that play a key role in temperature entrainment of the circadian clock in Arabidopsis.
Pseudo-response regulators are so named because they lack an Asp residue that is conserved in the receiver domain of typical two-component response regulators and is phosphorylated by the kinase partner of the two-component system (Hwang et al., 2002 ). Makino et al. (2000) showed that the receiver-like domains of TOC1 and PRR2 do not appear to have phosphate-accepting activity in vitro, so the mechanism of action of the PRR proteins remains unclear.
Salomé and McClung studied output rhythms of cotyledon movements and also the expression in transgenic plants of the reporter gene LUCIFERASE driven (individually) by the promoters of the clock-regulated genes CCA1, TOC1, LHY, PRR7, and PRR9. They show that these output rhythms can be reset or entrained by thermocycles (i.e., alternating warm and cool conditions). They next analyzed the response of prr3, prr5, prr7, and prr9 single mutants to a range of entraining thermocycles and found that prr7 and prr9 mutants were strongly affected, whereas prr3 and prr5 mutants were minimally affected in their response to thermocycles. In addition, prr7 prr9 double mutant plants lost the ability to reset the clock in response to temperature entrainment and failed to maintain rhythmicity in the dark. Interestingly, they also found that, in the absence of thermocycles, loss-of-function alleles of PRR3 and PRR5 shortened clock period (similar to what Más et al. [ 2003b]
The results of Salomé and McClung as well as those recently reported by Farré et al. (2005)
Alabadí, D., Yanovsky, M.J., Más, P., Harmer, S.L., and Kay, S.A. (2001). Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr. Biol. 12, 757–761. Albrecht, U., and Eichele, G. (2003). The mammalian circadian clock. Curr. Opin. Genet. Dev. 13, 271–277.[CrossRef][ISI][Medline] Coleman, R.M. (1986). Wide Awake at 3:00 a.m.: By Choice or by Chance? (New York: W.H. Freeman and Co.). Devlin, P.F., and Kay, S.A. (2001). Circadian photoperception. Annu. Rev. Physiol. 63, 677–694.[CrossRef][ISI][Medline] Farré, E.M., Harmer, S.L., Harmon, F.G., Yanovsky, M.J., and Kay, S.A. (2005). Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15, 47–54.[CrossRef][ISI][Medline] Han, L., Mason, M., Risseeuw, E.P., Crosby, W.L., and Somers, D.E. (2004). Formation of an SCFZTL complex is required for proper regulation of circadian timing. Plant J. 40, 291–301.[CrossRef][ISI][Medline]
Hwang, I., Chen, H.-C., and Sheen, J. (2002). Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 129, 500–515. Jarillo, J.A., Capel, J., Tang, R.-H., Yang, H.-Q., Alonso, J.M., Ecker, J.R., and Cashmore, A.R. (2001). An Arabidopsis circadian clock component interacts with both CRY1 and phyB. Nature 410, 487–490.[CrossRef][Medline] Makino, S., Kiba, T., Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Ueguchi, C., Sugiyama, T., and Mizuno, T. (2000). Genes encoding pseudo-response regulators: Insights into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 41, 791–803.
Más, P., Alabadí, D., Yanovsky, M.J., Oyama, T., and Kay, S.A. (2003b). Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15, 223–236. Más, P., Kim, W.-Y., Somers, D.E., and Kay, S.A. (2003a). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567–570.[CrossRef][Medline]
Matsushika, A., Makino, S., Kojima, M., and Mizuno, T. (2000). Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: Insight into the plant circadian clock. Plant Cell Physiol. 41, 1002–1012. McClung, C.R., Salomé, P.A., and Michael, T.P. (2002). The Arabidopsis circadian system. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0044, http://www.aspb.org/publications/arabidopsis/. Mizuno, T. (2004). Plant response regulators implicated in signal transduction and circadian rhythm. Curr. Opin. Plant Biol. 7, 499–505.[CrossRef][ISI][Medline] Pittendrigh, C.S. (1993). Temporal organization: Reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55, 17–54.[CrossRef]
Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. (2002). The orphan nuclear receptor REV-ERB
Salomé, P.A., and McClung, C.R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17, 791–803. Yagita, K., Tamanini, F., Yasuda, M., Hoeijmakers, J.H., van der Horst, G.T., and Okamura, H. (2002). Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J. 21, 1301–1314.[CrossRef][ISI][Medline] Related articles in Plant Cell:
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1 min, or 1/1000) (Pittendrigh, 1993
TOP
HOW CLOCKS WORK
CLOCK ENTRAINMENT
. These gene products, in turn, inhibit CLOCK/BMAL1 and thereby negatively regulate their own transcription (see 