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      The LDL1/2-HDA6 Histone Modification Complex Interacts With TOC1 and Regulates the Core Circadian Clock Components in Arabidopsis

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          Abstract

          In Arabidopsis, the circadian rhythm is associated with multiple important biological processes and maintained by multiple interconnected loops that generate robust rhythms. The circadian clock central loop is a negative feedback loop composed of the core circadian clock components. TOC1 ( TIMING OF CAB EXPRESSION 1) is highly expressed in the evening and negatively regulates the expression of CCA1 ( CIRCADIAN CLOCK ASSOCIATED 1)/ LHY ( LATE ELONGATED HYPOCOTYL). CCA1/LHY also binds to the promoter of TOC1 and represses the TOC1 expression. Our recent research revealed that the histone modification complex comprising of LYSINE-SPECIFIC DEMETHYLASE 1 (LSD1)-LIKE 1/2 (LDL1/2) and HISTONE DEACETYLASE 6 (HDA6) can be recruited by CCA1/LHY to repress TOC1 expression. In this study, we found that HDA6, LDL1, and LDL2 can interact with TOC1, and the LDL1/2-HDA6 complex is associate with TOC1 to repress the CCA1/LHY expression. Furthermore, LDL1/2-HDA6 and TOC1 co-target a subset of genes involved in the circadian rhythm. Collectively, our results indicate that the LDL1/2-HDA6 histone modification complex is important for the regulation of the core circadian clock components.

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          Most cited references35

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          Peroxiredoxins are conserved markers of circadian rhythms

          Summary Cellular life emerged ~3.7 billion years ago. With scant exception, terrestrial organisms have evolved under predictable daily cycles due to the Earth’s rotation. The advantage conferred upon organisms that anticipate such environmental cycles has driven the evolution of endogenous circadian rhythms that tune internal physiology to external conditions. The molecular phylogeny of mechanisms driving these rhythms has been difficult to dissect because identified clock genes and proteins are not conserved across the domains of life: Bacteria, Archaea and Eukaryota. Here we show that oxidation-reduction cycles of peroxiredoxin proteins constitute a universal marker for circadian rhythms in all domains of life, by characterising their oscillations in a variety of model organisms. Furthermore, we explore the interconnectivity between these metabolic cycles and transcription-translation feedback loops of the clockwork in each system. Our results suggest an intimate co-evolution of cellular time-keeping with redox homeostatic mechanisms following the Great Oxidation Event ~2.5 billion years ago.
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            Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.

            The interactive regulation between clock genes is central for oscillator function. Here, we show interactions between the Arabidopsis clock genes LATE ELONGATED HYPOCOTYL (LHY), CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), and TIMING OF CAB EXPRESSION 1 (TOC1). The MYB transcription factors LHY and CCA1 negatively regulate TOC1 expression. We show that both proteins bind to a region in the TOC1 promoter that is critical for its clock regulation. Conversely, TOC1 appears to participate in the positive regulation of LHY and CCA1 expression. Our results indicate that these interactions form a loop critical for clock function in Arabidopsis.
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              Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.

              The CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene encodes a MYB-related transcription factor involved in the phytochrome induction of a light-harvesting chlorophyll a/b-protein (Lhcb) gene. Expression of the CCA1 gene is transiently induced by phytochrome and oscillates with a circadian rhythm. Constitutive expression of CCA1 protein in transgenic plants abolished the circadian rhythm of several genes with dramatically different phases. These plants also had longer hypocotyls and delayed flowering, developmental processes regulated by light and the circadian clock. Furthermore, the expression of both endogenous CCA1 and the related LHY gene was suppressed. Our results suggest that CCA1 is a part of a feedback loop that is closely associated with the circadian clock in Arabidopsis.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                26 February 2019
                2019
                : 10
                : 233
                Affiliations
                [1] 1Institute of Plant Biology, National Taiwan University , Taipei, Taiwan
                [2] 2Agriculture and Agri-Food Canada, London Research and Development Centre , London, ON, Canada
                [3] 3Department of Biology, Western University , London, ON, Canada
                [4] 4State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resource, School of Life Sciences, Sun Yat-sen University , Guangzhou, China
                Author notes

                Edited by: Jean-Benoit Charron, McGill University, Canada

                Reviewed by: R. Glen Uhrig, University of Alberta, Canada; Jun Xiao, Institute of Genetics and Developmental Biology (CAS), China

                *Correspondence: Yuhai Cui, Yuhai.cui@ 123456canada.ca Keqiang Wu, kewu@ 123456ntu.edu.tw

                This article was submitted to Plant Cell Biology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.00233
                6399392
                30863422
                05c9e1db-b64c-4b4c-b4cc-6b8733238f17
                Copyright © 2019 Hung, Chen, Li, Chen, Chen, Cui and Wu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 25 October 2018
                : 12 February 2019
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 45, Pages: 10, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                h3k4 demethylases,hda6,circadian clock,cca1/lhy,toc1,arabidopsis
                Plant science & Botany
                h3k4 demethylases, hda6, circadian clock, cca1/lhy, toc1, arabidopsis

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