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Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids

Author

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  • Xiaoli Shi

    (Section of Molecular Cell and Developmental Biology, Center for Computational Biology and Bioinformatics, and Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station, A4800, Austin, Texas 78712, USA.)

  • Danny W-K. Ng

    (Section of Molecular Cell and Developmental Biology, Center for Computational Biology and Bioinformatics, and Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station, A4800, Austin, Texas 78712, USA.)

  • Changqing Zhang

    (Section of Molecular Cell and Developmental Biology, Center for Computational Biology and Bioinformatics, and Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station, A4800, Austin, Texas 78712, USA.)

  • Luca Comai

    (Plant Biology and Genome Center, University of California, 451 Health Sciences Drive, Davis, Davis, California 95616, USA.)

  • Wenxue Ye

    (State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University)

  • Z. Jeffrey Chen

    (Section of Molecular Cell and Developmental Biology, Center for Computational Biology and Bioinformatics, and Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station, A4800, Austin, Texas 78712, USA.
    State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University)

Abstract

Gene-expression divergence between species shapes morphological evolution, but the molecular basis is largely unknown. Here we show cis- and trans-regulatory elements and chromatin modifications on gene-expression diversity in genetically tractable Arabidopsis allotetraploids. In Arabidopsis thaliana and Arabidopsis arenosa, both cis and trans with predominant cis-regulatory effects mediate gene-expression divergence. The majority of genes with both cis- and trans-effects are subjected to compensating interactions and stabilizing selection. Interestingly, cis- and trans-regulation is associated with chromatin modifications. In F1 allotetraploids, Arabidopsis arenosa trans factors predominately affect allelic expression divergence. Arabidopsis arenosa trans factors tend to upregulate Arabidopsis thaliana alleles, whereas Arabidopsis thaliana trans factors up- or down-regulate Arabidopsis arenosa alleles. In resynthesized and natural allotetraploids, trans effects drive expression of both homoeologous loci into the same direction. We provide evidence for natural selection and chromatin regulation in shaping gene-expression diversity during plant evolution and speciation.

Suggested Citation

  • Xiaoli Shi & Danny W-K. Ng & Changqing Zhang & Luca Comai & Wenxue Ye & Z. Jeffrey Chen, 2012. "Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids," Nature Communications, Nature, vol. 3(1), pages 1-9, January.
    • Handle: RePEc:nat:natcom:v:3:y:2012:i:1:d:10.1038_ncomms1954
    DOI: 10.1038/ncomms1954
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    Cited by:

    1. Karel Janko & Jan Eisner & Petr Cigler & Tomáš Tichopád, 2024. "Unifying framework explaining how parental regulatory divergence can drive gene expression in hybrids and allopolyploids," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Fei He & Wei Wang & William B. Rutter & Katherine W. Jordan & Jie Ren & Ellie Taagen & Noah DeWitt & Deepmala Sehgal & Sivakumar Sukumaran & Susanne Dreisigacker & Matthew Reynolds & Jyotirmoy Halder , 2022. "Genomic variants affecting homoeologous gene expression dosage contribute to agronomic trait variation in allopolyploid wheat," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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