Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock

Eriksson, Maria E.; Hanano, Shigeru; Southern, Megan M; Hall, Anthony; Millar, Andrew J.

doi:10.1007/s00425-003-1106-4

Cited by 90 publications

(74 citation statements)

References 16 publications

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“…Neither insertion allele displayed an altered rhythm under constant darkness, indicating that JMJD5 function is light-dependent (Table S2). Similar lightdependent circadian phenotypes have been reported for other clock mutations (24,25).…”

Section: Resultssupporting

confidence: 84%

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

Jones

Covington

DiTacchio

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

148

155

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Circadian clocks are near-ubiquitous molecular oscillators that coordinate biochemical, physiological, and behavioral processes with environmental cues, such as dawn and dusk. Circadian timing mechanisms are thought to have arisen multiple times throughout the evolution of eukaryotes but share a similar overall structure consisting of interlocking transcriptional and posttranslational feedback loops. Recent work in both plants and animals has also linked modification of histones to circadian clock function. Now, using data from published microarray experiments, we have identified a histone demethylase, jumonji domain containing 5 (JMJD5), as a previously undescribed participant in both the human and Arabidopsis circadian systems. Arabidopsis JMJD5 is coregulated with evening-phased clock components and positively affects expression of clock genes expressed at dawn. We found that both Arabidopsis jmjd5 mutant seedlings and mammalian cell cultures deficient for the human ortholog of this gene have similar fastrunning circadian oscillations compared with WT. Remarkably, both the Arabidopsis and human JMJD5 orthologs retain sufficient commonality to rescue the circadian phenotype of the reciprocal system. Thus, JMJD5 plays an interchangeable role in the timing mechanisms of plants and animals despite their highly divergent evolutionary paths.C ircadian rhythms are endogenous oscillations that attune the behavior and physiology of organisms to regular changes in their environment, such as dusk and dawn. It is estimated that 1/10th of mammalian genes and one-third of Arabidopsis genes are regulated in a circadian fashion (1, 2). Not surprisingly, the circadian clock modulates a broad range of processes, ranging from the regulation of growth and flowering time in plants to the control of body temperature and the sleep-wake cycle in mammals (3, 4). The coordination of these molecular and physiological processes with the external environment has been shown to provide an adaptive advantage in organisms as diverse as cyanobacteria, higher plants, and insects (5-7).Although it is thought that circadian clocks have arisen multiple times during eukaryotic evolution (8), molecular oscillators in a diverse range of lineages share a broad overall structure consisting of interlocking transcriptional and posttranslational feedback loops (3, 4). In plants, the morning-phased Myb-like transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) repress the expression of TIMING OF CAB1 EXPRESSION 1 (TOC1) by binding to a conserved motif within its promoter known as the evening element (9-11). TOC1, in turn, promotes expression of CCA1 and LHY via an indirect mechanism, forming a negative feedback loop (12). This central CCA1/LHY/TOC1 loop interlocks with additional morningand evening-phased circuits to provide more robustness and flexibility to the circadian mechanism (reviewed in 3, 13).Because genes that act together are often coregulated (14), we have characterized a gene that is coexpressed with TO...

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Section: Resultssupporting

confidence: 84%

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

Jones

Covington

DiTacchio

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

148

155

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“…Both GI and LUX, evening-expressed regulators of CCA1/LHY (Fowler et al 1999;Hazen et al 2005), lost rhythmic amplitude in the triple mutant after one constant-light cycle (Figure 2, A and B). Similarly, PRR9, a morning-clock gene (Matsushika et al 2000;Makino et al 2002;Eriksson et al 2003), exhibited markedly , cca1-11, lhy-21, toc1-21, cca1-11 lhy-21, cca1-11 toc1-21, lhy-21 toc1-21, and cca1-11 lhy-21 toc1-21 was measured under standard 8L/16D conditions. Mean leaf number is shown 6SE (n ¼ 30-40).…”

Section: Discussionmentioning

confidence: 95%

“…They act on the proposed positive-activator termed TIMING OF CAB EXPRES-SION 1 (TOC1); it works in the evening and encodes a protein of unknown biochemical activity (Somers et al 1998a;Strayer et al 2000;Alabadi et al 2001). TOC1 belongs to the PRR (PSEUDO-RESPONSE REG-ULATOR) family of proteins, consisting of five members (PRR9, PRR7, PRR5, PRR3, and PRR1/TOC1) (Matsushika et al 2000;Makino et al 2002;Eriksson et al 2003). TOC1 and CCA1/LHY together make up the proposed central circadian loop in Arabidopsis.…”

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confidence: 99%

A Complex Genetic Interaction BetweenArabidopsis thalianaTOC1 and CCA1/LHY in Driving the Circadian Clock and in Output Regulation

et al. 2007

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It has been proposed that CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) together with TIMING OF CAB EXPRESSION 1 (TOC1) make up the central oscillator of the Arabidopsis thaliana circadian clock. These genes thus drive rhythmic outputs, including seasonal control of flowering and photomorphogenesis. To test various clock models and to disclose the genetic relationship between TOC1 and CCA1/LHY in floral induction and photomorphogenesis, we constructed the cca1 lhy toc1 triple mutant and cca1 toc1 and lhy toc1 double mutants and tested various rhythmic responses and circadian output regulation. Here we report that rhythmic activity was dramatically attenuated in cca1 lhy toc1. Interestingly, we also found that TOC1 regulates the floral transition in a CCA1/LHY-dependent manner while CCA1/LHY functions upstream of TOC1 in regulating a photomorphogenic process. This suggests to us that TOC1 and CCA1/LHY participate in these two processes through different strategies. Collectively, we have used genetics to provide direct experimental support of previous modeling efforts where CCA1/LHY, along with TOC1, drives the circadian oscillator and have shown that this clock is essential for correct output regulation.

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“…PRR single mutants were found to cause a mild effect on period length, whereas some double and triple mutant combinations result in a severe clock phenotype: the double mutant prr9 prr7 displayed a longer period than either of the single mutants, and the prr5 prr7 double mutant phenotype was reported to exhibit very short to arrhythmic oscillations that became further compromised in the prr9 prr7 prr5 triple mutant (Farre et al, 2005;Fujimori et al, 2005;Nakamichi et al, 2005aNakamichi et al, , 2005bSalome and McClung, 2005). Interestingly, combining the clock phenotype of the short-period prr5 mutation with the long-period prr9 mutation resulted in a wild-type period (Eriksson et al, 2003). Hence, despite their molecular similarity, not all PRRs are functionally equivalent, although some may have overlapping functions.…”

Section: Introductionmentioning

confidence: 99%

PRR3 Is a Vascular Regulator of TOC1 Stability in theArabidopsisCircadian Clock

et al. 2007

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The pseudoresponse regulators (PRRs) participate in the progression of the circadian clock in Arabidopsis thaliana. The founding member of the family, TIMING OF CAB EXPRESSION1 (TOC1), is an essential component of the transcriptional network that constitutes the core mechanism of the circadian oscillator. Recent data suggest a role in circadian regulation for all five members of the PRR family; however, the molecular function of TOC1 or any other PRRs remains unknown. In this work, we present evidence for the involvement of PRR3 in the regulation of TOC1 protein stability. PRR3 was temporally coexpressed with TOC1 under different photoperiods, yet its tissue expression was only partially overlapping with that of TOC1, as PRR3 appeared restricted to the vasculature. Decreased expression of PRR3 resulted in reduced levels of TOC1 protein, while overexpression of PRR3 caused an increase in the levels of TOC1, all without affecting the amount of TOC1 transcript. PRR3 was able to bind to TOC1 in yeast and in plants and to perturb TOC1 interaction with ZEITLUPE (ZTL), which targets TOC1 for proteasome-dependent degradation. Together, our results indicate that PRR3 might function to modulate TOC1 stability by hindering ZTL-dependent TOC1 degradation, suggesting the existence of local regulators of clock activity and adding to the growing importance of posttranslational regulation in the design of circadian timing mechanisms in plants.

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Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock

Cited by 90 publications

References 16 publications

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

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

A Complex Genetic Interaction BetweenArabidopsis thalianaTOC1 and CCA1/LHY in Driving the Circadian Clock and in Output Regulation

PRR3 Is a Vascular Regulator of TOC1 Stability in theArabidopsisCircadian Clock

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