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      Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids

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          Abstract

          Segregating hybrids and stable allopolyploids display morphological vigor 1, 2, 3, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and A. arenosa 1, 4. The mechanisms are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants 5, 6, 7, 8. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 ( CCA1) and LATE ELONGATED HYPOCOTYL ( LHY) 9, 10 and their reciprocal regulators TIMING OF CAB EXPRESSION 1 ( TOC1) and GIGANTEA ( GI) 10, 11, 12 mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced expression of TOC1, GI and downstream genes that contain CCA1 binding site (CBS) 13 in chlorophyll and starch metabolic pathways in allotetraploids and F 1 hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and daily repression of cca1 in TOC1:cca1-RNAi transgenic plants increased expression of downstream genes and chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1:CCA1 had the opposite effects. The causal effects of CCA1 on output traits suggest that hybrids and allopolyploids gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigor and increased biomass.

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          Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.

          D Alabadí, T Oyama, M Yanovsky … (2001)
          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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            Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.

            Z. Jeffrey Chen (2007)
            Polyploidy, or whole-genome duplication (WGD), is an important genomic feature for all eukaryotes, especially many plants and some animals. The common occurrence of polyploidy suggests an evolutionary advantage of having multiple sets of genetic material for adaptive evolution. However, increased gene and genome dosages in autopolyploids (duplications of a single genome) and allopolyploids (combinations of two or more divergent genomes) often cause genome instabilities, chromosome imbalances, regulatory incompatibilities, and reproductive failures. Therefore, new allopolyploids must establish a compatible relationship between alien cytoplasm and nuclei and between two divergent genomes, leading to rapid changes in genome structure, gene expression, and developmental traits such as fertility, inbreeding, apomixis, flowering time, and hybrid vigor. Although the underlying mechanisms for these changes are poorly understood, some themes are emerging. There is compelling evidence that changes in DNA sequence, cis- and trans-acting effects, chromatin modifications, RNA-mediated pathways, and regulatory networks modulate differential expression of homoeologous genes and phenotypic variation that may facilitate adaptive evolution in polyploid plants and domestication in crops.
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              Circadian rhythms from flies to human.

              Satchidananda Panda, John B. Hogenesch, Steve A Kay (2002)
              In this era of jet travel, our body 'remembers' the previous time zone, such that when we travel, our sleep wake pattern, mental alertness, eating habits and many other physiological processes temporarily suffer the consequences of time displacement until we adjust to the new time zone. Although the existence of a circadian clock in humans had been postulated for decades, an understanding of the molecular mechanisms has required the full complement of research tools. To gain the initial insights into circadian mechanisms, researchers turned to genetically tractable model organisms such as Drosophila.
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 0410462
                Journal ID (pubmed-jr-id): 6011
                Journal ID (nlm-ta): Nature
                Title: Nature
                ISSN (Print): 0028-0836
                ISSN (Electronic): 1476-4687
                Publication date Nihms-submitted: 7 October 2008
                Publication date (Electronic): 23 November 2008
                Publication date (Print): 15 January 2009
                Publication date PMC-release: 15 July 2009
                Volume: 457
                Issue: 7227
                Pages: 327-331
                Affiliations
                [1 ]Section of Molecular Cell and Developmental Biology, The University of Texas at Austin, One University Station, A-4800, Austin, TX 78712, USA
                [2 ]Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station, A-4800, Austin, TX 78712, USA
                [3 ]Center for Computational Biology and Bioinformatics, The University of Texas at Austin, One University Station, A-4800, Austin, TX 78712, USA
                [4 ]Section of Integrative Biology, The University of Texas at Austin, One University Station, A-4800, Austin, TX 78712, USA
                Author notes
                [*]

                These two authors contributed equally to the work.

                [†]

                Present address: Department of Plant Genetics and Breeding, China Agricultural University, Yuanmingyuan Xilu No. 2, Beijing, 100094, China

                Author Contributions Z.N. examined gene expression, ChIP, chlorophyll, starch, and sugars in allotetraploids and hybrids. E.D.K. analyzed CCA1 mRNA, protein, chlorophyll and starch in the transgenic plants and mutants. M.H. conducted statistical tests. E.L. performed EMSA. J.L. assayed Western and ChIP. Y.Z. assisted cloning. Q.S. discussed the experiments. Z.J.C. conceived the project, analyzed the data, and wrote the paper.

                [‡ ]Corresponding author: The University of Texas at Austin, Institute for Cellular and Molecular Biology, One University Station, A4800, Austin, TX 78712−0183, USA Phone: 512−475−9327; Fax: 512−471−2149; Email: zjchen@ 123456mail.utexas.edu
                Article
                Manuscript ID: nihpa72865
                DOI: 10.1038/nature07523
                PMC ID: 2679702
                PubMed ID: 19029881
                SO-VID: 60ba9cf7-d1d9-44e7-b27e-fc1abc3cca73
                History
                Funding
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: R01 GM067015-06 ||GM
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: R01 GM067015-05 ||GM
                Funded by: National Institute of General Medical Sciences : NIGMS
                Award ID: R01 GM067015-04 ||GM
                Categories
                Subject: Article

                ScienceOpen disciplines: Uncategorized
                Keywords: epigenetics,hybrid vigor,polyploidy,biomass,circadian clock,gene expression
                Data availability:
                ScienceOpen disciplines: Uncategorized
                Keywords: epigenetics, hybrid vigor, polyploidy, biomass, circadian clock, gene expression

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