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Unifying framework explaining how parental regulatory divergence can drive gene expression in hybrids and allopolyploids

Author

Listed:
  • Karel Janko

    (Rumburská 89)

  • Jan Eisner

    (Branišovská 1760
    Chittussiho 10)

  • Petr Cigler

    (166 10)

  • Tomáš Tichopád

    (Chittussiho 10
    389 25)

Abstract

Hybridization and polyploidy are powerful evolutionary forces, inducing a range of phenotypic outcomes, including non-additive expression, subgenome dominance, deviations in genomic dosage, and transcriptome downsizing. The reasons for these patterns and whether they are universal adaptive responses to genome merging and doubling remain debated. To address this, we develop a thermodynamic model of gene expression based on transcription factor (TF)-promoter binding. Applied to hybridization between species with divergent gene expression levels, cell volumes, or euchromatic ratios, this model distinguishes the effects of hybridization from those of polyploidy. Our results align with empirical observations, suggesting that gene regulation patterns in hybrids and polyploids often stem from the constrained interplay between inherited diverged regulatory networks rather than from subsequent adaptive evolution. In addition, occurrence of certain phenotypic traits depend on specific assumptions about promoter-TF coevolution and their distribution within the hybrid’s nucleoplasm, offering new research avenues to understand the underlying mechanisms. In summary, our model explains how the legacy of divergent species directly influences the phenotypic traits of hybrids and allopolyploids.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52546-5
    DOI: 10.1038/s41467-024-52546-5
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    References listed on IDEAS

    as
    1. 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.
    2. Annie E. Tsong & Brian B. Tuch & Hao Li & Alexander D. Johnson, 2006. "Evolution of alternative transcriptional circuits with identical logic," Nature, Nature, vol. 443(7110), pages 415-420, September.
    3. Patricia J. Wittkopp & Belinda K. Haerum & Andrew G. Clark, 2004. "Evolutionary changes in cis and trans gene regulation," Nature, Nature, vol. 430(6995), pages 85-88, July.
    4. Xinru Zhang & Bohao Fang & Yi-Fei Huang, 2023. "Transcription factor binding sites are frequently under accelerated evolution in primates," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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