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      The ELF4-ELF3-LUX Complex Links the Circadian Clock to Diurnal Control of Hypocotyl Growth

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          Abstract

          The circadian clock is required for adaptive responses to daily and seasonal changes in environmental conditions 1- 3 . Light and the circadian clock interact to consolidate the phase of hypocotyl cell elongation to dawn under diurnal cycles in Arabidopsis thaliana 4- 7 . Here we identify a protein complex (Evening Complex) composed of EARLY FLOWERING 3 (ELF3), EARLY FLOWERING 4 (ELF4) and the transcription factor LUX ARRHYTHMO (LUX) that directly regulates plant growth 8- 12 . ELF3 is both necessary and sufficient to form a complex between ELF4 and LUX, and the complex is diurnally regulated, peaking at dusk. ELF3, ELF4 and LUX are required for the proper expression of the growth-promoting transcription factors PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and PIF5 under diurnal conditions 4, 6, 13 . LUX targets the complex to the promoters of PIF4 and PIF5 in vivo. Mutations in PIF4 and/or PIF5 are epistatic to the loss of the ELF4-ELF3-LUX complex, suggesting that regulation of PIF4 and PIF5 is a critical function of the complex. Therefore, the Evening Complex underlies the molecular basis for circadian gating of hypocotyl growth in the early evening.

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          Most cited references18

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          FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis.

          Precise timing of CONSTANS (CO) gene expression is necessary for day-length discrimination for photoperiodic flowering. The FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1), and GIGANTEA (GI) proteins regulate CO transcription in Arabidopsis. We demonstrate that FKF1 and GI proteins form a complex in a blue-light-dependent manner. The timing of this interaction regulates the timing of daytime CO expression. FKF1 function is dependent on GI, which interacts with a CO repressor, CYCLING DOF FACTOR 1 (CDF1), and controls CDF1 stability. GI, FKF1, and CDF1 proteins associate with CO chromatin. Thus, the FKF1-GI complex forms on the CO promoter in late afternoon to regulate CO expression, providing a mechanistic view of how the coincidence of light with circadian timing regulates photoperiodic flowering.
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            Rhythmic growth explained by coincidence between internal and external cues.

            Most organisms use circadian oscillators to coordinate physiological and developmental processes such as growth with predictable daily environmental changes like sunrise and sunset. The importance of such coordination is highlighted by studies showing that circadian dysfunction causes reduced fitness in bacteria and plants, as well as sleep and psychological disorders in humans. Plant cell growth requires energy and water-factors that oscillate owing to diurnal environmental changes. Indeed, two important factors controlling stem growth are the internal circadian oscillator and external light levels. However, most circadian studies have been performed in constant conditions, precluding mechanistic study of interactions between the clock and diurnal variation in the environment. Studies of stem elongation in diurnal conditions have revealed complex growth patterns, but no mechanism has been described. Here we show that the growth phase of Arabidopsis seedlings in diurnal light conditions is shifted 8-12 h relative to plants in continuous light, and we describe a mechanism underlying this environmental response. We find that the clock regulates transcript levels of two basic helix-loop-helix genes, phytochrome-interacting factor 4 (PIF4) and PIF5, whereas light regulates their protein abundance. These genes function as positive growth regulators; the coincidence of high transcript levels (by the clock) and protein accumulation (in the dark) allows them to promote plant growth at the end of the night. Thus, these two genes integrate clock and light signalling, and their coordinated regulation explains the observed diurnal growth rhythms. This interaction may serve as a paradigm for understanding how endogenous and environmental signals cooperate to control other processes.
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              COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability.

              Seasonal changes in day length are perceived by plant photoreceptors and transmitted to the circadian clock to modulate developmental responses such as flowering time. Blue-light-sensing cryptochromes, the E3 ubiquitin-ligase COP1, and clock-associated proteins ELF3 and GI regulate this process, although the regulatory link between them is unclear. Here we present data showing that COP1 acts with ELF3 to mediate day length signaling from CRY2 to GI within the photoperiod flowering pathway. We found that COP1 and ELF3 interact in vivo and show that ELF3 allows COP1 to interact with GI in vivo, leading to GI degradation in planta. Accordingly, mutation of COP1 or ELF3 disturbs the pattern of GI cyclic accumulation. We propose a model in which ELF3 acts as a substrate adaptor, enabling COP1 to modulate light input signal to the circadian clock through targeted destabilization of GI.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                2 August 2011
                13 July 2011
                21 January 2012
                : 475
                : 7356
                : 398-402
                Affiliations
                [1 ]Section of Cell & Developmental Biology, Division of Biological Sciences, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0130, USA
                [2 ]Center for Chronobiology, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0130, USA
                Author notes
                [3]

                Present address: Department of Biology, University of Washington, 24 Kincaid Hall, Box 351800, Seattle, WA, 98195-1800, USA

                [4]

                Present address: Nicholas School of the Environment, Duke University Marine Laboratory, 135 Duke Marine Lab Rd, Beaufort, NC 28516, USA

                [5]

                Present address: Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA

                Article
                nihpa313091
                10.1038/nature10182
                3155984
                21753751
                6b4463b1-6d6d-49d9-b461-eb98c210ad95

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                History
                Funding
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: RC2 GM092412-02 || GM
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: R01 GM067837-09 || GM
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: R01 GM056006-16 || GM
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: F32 GM083585-03 || GM
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