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MBE Advance Access originally published online on July 31, 2009
Molecular Biology and Evolution 2009 26(11):2533-2538; doi:10.1093/molbev/msp171
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Roles of Trans and Cis Variation in Yeast Intraspecies Evolution of Gene Expression

Huang-Mo Sung*,{dagger},1, Tzi-Yuan Wang*,1, Daryi Wang{ddagger}, Yu-Shan Huang§, Jen-Pey Wu§, Huai-Kuang Tsai||, Jengnan Tzeng*, Chih-Jen Huang*, Yi-Chen Lee*, Peggy Yang*, Joyce Hsu*, Tiffany Chang*, Chung-Yi Cho||, Li-Chuan Weng{ddagger}, Tso-Ching Lee§, Tien-Hsien Chang*, Wen-Hsiung Li*,{ddagger},# and Ming-Che Shih**,{dagger}{dagger}

* Genomics Research Center, Academia Sinica, Taipei, Taiwan
{dagger} Department of Life Sciences, National Cheng Kung University, Tainan, Taiwan
{ddagger} Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
§ Department of Medical Research, Taichung Veterans General Hospital, Taichung, Taiwan
|| Institute of Information Science, Academia Sinica, Taipei, Taiwan
Department of Molecular Genetics, The Ohio State University
# Department of Ecology and Evolution, University of Chicago
** Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan
{dagger}{dagger} Department of Biology, University of Iowa

E-mail: mcshih{at}gate.sinica.edu.tw.

Accepted for publication July 22, 2009.

Both cis and trans mutations contribute to gene expression divergence within and between species. We used Saccharomyces cerevisiae as a model organism to estimate the relative contributions of cis and trans variations to the expression divergence between a laboratory (BY) and a wild (RM) strain of yeast. We examined whether genes regulated by a single transcription factor (TF; single input module, SIM genes) or genes regulated by multiple TFs (multiple input module, MIM genes) are more susceptible to trans variation. Because a SIM gene is regulated by a single immediate upstream TF, the chance for a change to occur in its trans-acting factors would, on average, be smaller than that for a MIM gene. We chose 232 genes that exhibited expression divergence between BY and RM to test this hypothesis. We examined the expression patterns of these genes in a BY–RM coculture system and in a BY–RM diploid hybrid. We found that trans variation is far more important than cis variation for expression divergence between the two strains. However, because in 75% of the genes studied, cis variation has significantly contributed to expression divergence, cis change also plays a significant role in intraspecific expression evolution. Interestingly, we found that the proportion of genes with diverged expression between BY and RM is larger for MIM genes than for SIM genes; in fact, the proportion tends to increase with the number of transcription factors that regulate the gene. Moreover, MIM genes are, on average, subject to stronger trans effects than SIM genes, though the difference between the two types of genes is not conspicuous.

Key Words: cis-regulation • trans-regulation • yeast • expression evolution


1 These two authors contributed equally to the paper.

Takashi Gojobori, Associate Editor


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