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Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids

Nature volume 457, pages 327–331 (2009)Cite this article

Abstract

Segregating hybrids and stable allopolyploids display morphological vigour1,2,3, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and Arabidopsis arenosa1,4—the mechanisms for this are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants5,6,7,8. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY)9,10,11 and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI)10,12,13 mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced the expression of TOC1, GI and downstream genes containing evening elements14 in chlorophyll and starch metabolic pathways in allotetraploids and F1 hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and the daily repression of cca1 by RNA interference (RNAi) in TOC1::cca1(RNAi) transgenic plants increased the expression of downstream genes and increased chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1::CCA1 had the opposite effect. 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 vigour and increased biomass.

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Figure 1: Locus-specific and chromatin regulation of circadian clock genes in the allotetraploids.
Figure 2: Increase in chlorophyll content and upregulation of the genes involved in chlorophyll and starch biosynthesis in allotetraploids.
Figure 3: CCA1 function and increased amounts of chlorophyll, starch and sugar in allotetraploids and F 1 hybrids.
Figure 4: A role of CCA1 in growth vigour in allotetraploids and hybrids.

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Acknowledgements

We are grateful to E. Tobin for her gifts of the CCA1-overexpression (CCA1-OX) line and antibodies against CCA1. We thank H. Y. Chen for advice on recombinant CCA1 production, D. W. Ng for western blot analysis, T. Juenger for insightful discussions on life history traits in Arabidopsis, and D. Y. Chen and E. Huq for careful readings of the manuscript. The work was supported by the grants from the National Science Foundation Plant Genome Research Program (DBI0733857 and DBI0624077) and the National Institutes of Health (GM067015; Z.J.C.) and National Basic Research Program of China (2007CB109000; Q.S.).

Author Contributions Z.N. examined gene expression, ChIP, chlorophyll, starch and sugars in allotetraploids and hybrids. E.-D.K. analysed 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 blots and ChIP. Y.Z. assisted cloning. Q.S. discussed the experiments. Z.J.C. conceived the project, analysed the data and wrote the paper.

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Author notes

  1. Zhongfu Ni & Yirong Zhang

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

  2. Zhongfu Ni and Eun-Deok Kim: These authors contributed equally to this work.

Authors and Affiliations

  1. Section of Molecular Cell and Developmental Biology,,

    Zhongfu Ni, Eun-Deok Kim, Misook Ha, Erika Lackey, Jianxin Liu, Yirong Zhang & Z. Jeffrey Chen

  2. Institute for Cellular and Molecular Biology,,

    Misook Ha & Z. Jeffrey Chen

  3. Center for Computational Biology and Bioinformatics, and,,

    Misook Ha & Z. Jeffrey Chen

  4. Section of Integrative Biology, The University of Texas at Austin, One University Station, A-4800, Austin, Texas 78712, USA ,

    Z. Jeffrey Chen

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

    Qixin Sun

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Ni, Z., Kim, ED., Ha, M. et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327–331 (2009). https://doi.org/10.1038/nature07523

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