Expression evolution in yeast genes of single-input modules is mainly due to changes in trans-acting factors

  1. Daryi Wang1,6,
  2. Huang-Mo Sung2,6,
  3. Tzi-Yuan Wang2,
  4. Chih-Jen Huang2,
  5. Peggy Yang2,
  6. Tiffany Chang2,
  7. Yang-Chao Wang2,
  8. Da-Lun Tseng2,
  9. Jen-Pey Wu3,
  10. Tso-Ching Lee3,
  11. Ming-Che Shih4, and
  12. Wen-Hsiung Li2,5,7
  1. 1 Research Center for Biodiversity, Academia Sinica, Taipei 115, Taiwan;
  2. 2 Genomics Research Center, Academia Sinica, Taipei 115, Taiwan;
  3. 3 Department of Medical Research, Taichung Veterans General Hospital, Taichung 407, Taiwan;
  4. 4 Department of Biological Sciences and Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa 52242, USA;
  5. 5 Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA
  1. 6 These authors contributed equally to this work.

Abstract

Both cis- and trans-regulatory mutations contribute to gene expression divergence within and between species. To estimate their relative contributions, we examined two yeast strains, BY (a laboratory strain) and RM (a wild strain), for their gene-expression divergence by microarray. Using these data and published ChIP-chip data, we obtained a set of single-regulator-regulated genes that showed expression divergence between BY and RM. We randomly selected 50 of these genes for further study. We developed a step-by-step approach to assess the relative contributions of cis- and trans-variations to expression divergence by using pyrosequencing to quantify the mRNA levels of the BY and RM alleles in the same culture (co-culture) and in hybrid diploids. Forty genes showed expression divergence between the two strains in co-culture, and pyrosequencing of the BY/RM hybrid diploids showed that 45% (18/40) can be attributed to differences in trans-acting factors alone, 17.5% (7/40) mainly to trans-variations, 20% (8/40) to both cis- and trans-acting factors, 7.5% (3/40) mainly to cis-variations, and 10% (4/40) to cis-acting factors alone. In addition, we replaced the BY promoter by the RM promoter in each of 10 BY genes that were found from our microarray data to have expression divergence between BY and RM, and in each case our quantitative PCR analysis revealed a cis effect of the promoter replacement on gene expression. In summary, our study suggests that trans-acting factors play the major role in expression evolution between yeast strains, but the role of cis variation is also important.

Footnotes

  • 7 Corresponding author.

    7 E-mail whli{at}uchicago.edu; fax (773) 702-9740.

  • [Supplemental material is available online at www.genome.org.]

  • Article published online before print. Article and publication date are online at http://www.genome.org/cgi/doi/10.1101/gr.6328907

    • Received January 25, 2007.
    • Accepted April 23, 2007.

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