Natural selection on cis and trans regulation in yeasts
- J.J. Emerson1,10,
- Li-Ching Hsieh1,2,10,
- Huang-Mo Sung3,10,
- Tzi-Yuan Wang1,4,10,
- Chih-Jen Huang4,5,6,
- Henry Horng-Shing Lu7,
- Mei-Yeh Jade Lu1,4,
- Shu-Hsing Wu8 and
- Wen-Hsiung Li1,4,9,11
- 1 Genomics Research Center, Academia Sinica, Taipei 115, Taiwan;
- 2 Institute of Information Science, Academia Sinica, Taipei 115, Taiwan;
- 3 Department of Life Sciences, National Cheng Kung University, Tainan 701, Taiwan;
- 4 Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan;
- 5 Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica, Taipei 115, Taiwan;
- 6 Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 402, Taiwan;
- 7 Institute of Statistics, National Chiao Tung University, Hsinchu 30010, Taiwan;
- 8 Institute of Plant and Microbial Biology, Academia Sinica, Taipei 115, Taiwan;
- 9 Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA
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↵10 These authors contributed equally to this work.
Abstract
Gene expression is regulated both by cis elements, which are DNA segments closely linked to the genes they regulate, and by trans factors, which are usually proteins capable of diffusing to unlinked genes. Understanding the patterns and sources of regulatory variation is crucial for understanding phenotypic and genome evolution. Here, we measure genome-wide allele-specific expression by deep sequencing to investigate the patterns of cis and trans expression variation between two strains of Saccharomyces cerevisiae. We propose a statistical modeling framework based on the binomial distribution that simultaneously addresses normalization of read counts derived from different parents and estimating the cis and trans expression variation parameters. We find that expression polymorphism in yeast is common for both cis and trans, though trans variation is more common. Constraint in expression evolution is correlated with other hallmarks of constraint, including gene essentiality, number of protein interaction partners, and constraint in amino acid substitution, indicating that both cis and trans polymorphism are clearly under purifying selection, though trans variation appears to be more sensitive to selective constraint. Comparing interspecific expression divergence between S. cerevisiae and S. paradoxus to our intraspecific variation suggests a significant departure from a neutral model of molecular evolution. A further examination of correlation between polymorphism and divergence within each category suggests that cis divergence is more frequently mediated by positive Darwinian selection than is trans divergence.
Footnotes
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↵11 Corresponding author.
E-mail whli{at}uchicago.edu; fax (773) 702-9740.
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[Supplemental material is available online at http://www.genome.org. The sequencing data from this study have been submitted to the NCBI Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo) under accession no. GSE20749.]
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Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.101576.109.
- Received October 7, 2009.
- Accepted April 1, 2010.
- Copyright © 2010 by Cold Spring Harbor Laboratory Press