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Evolutionary changes in cis and trans gene regulation

Author

Listed:
  • Patricia J. Wittkopp

    (Cornell University)

  • Belinda K. Haerum

    (Cornell University)

  • Andrew G. Clark

    (Cornell University)

Abstract

Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences1,2. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown3. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids4,5. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:430:y:2004:i:6995:d:10.1038_nature02698
    DOI: 10.1038/nature02698
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    Cited by:

    1. Jasper Panten & Tobias Heinen & Christina Ernst & Nils Eling & Rebecca E. Wagner & Maja Satorius & John C. Marioni & Oliver Stegle & Duncan T. Odom, 2024. "The dynamic genetic determinants of increased transcriptional divergence in spermatids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. 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.
    3. Jianping Quan & Ming Yang & Xingwang Wang & Gengyuan Cai & Rongrong Ding & Zhanwei Zhuang & Shenping Zhou & Suxu Tan & Donglin Ruan & Jiajin Wu & Enqin Zheng & Zebin Zhang & Langqing Liu & Fanming Men, 2024. "Multi-omic characterization of allele-specific regulatory variation in hybrid pigs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Matthew I. M. Louder & Hannah Justen & Abigail A. Kimmitt & Koedi S. Lawley & Leslie M. Turner & J. David Dickman & Kira E. Delmore, 2024. "Gene regulation and speciation in a migratory divide between songbirds," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Sarah E. Harris & Maria S. Alexis & Gilbert Giri & Francisco F. Cavazos & Yue Hu & Jernej Murn & Maria M. Aleman & Christopher B. Burge & Daniel Dominguez, 2024. "Understanding species-specific and conserved RNA-protein interactions in vivo and in vitro," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Jordi Planas & Josep M Serrat, 2010. "Gene Promoter Evolution Targets the Center of the Human Protein Interaction Network," PLOS ONE, Public Library of Science, vol. 5(7), pages 1-10, July.

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