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Differential paralog divergence modulates evolutionary outcomes in yeast

Monica R. Sanchez, Aaron W. Miller, Ivan Liachko, Anna B. Sunshine, Bryony Lynch, Mei Huang, Christopher G. DeSevo, Dave A. Pai, Cheryl M. Tucker, Margaret L. Hoang, Maitreya J. Dunham
doi: https://doi.org/10.1101/063248
Monica R. Sanchez
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
2Molecular and Cellular Biology Program, University of Washington, Seattle, Washington, United States of America
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Aaron W. Miller
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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Ivan Liachko
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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Anna B. Sunshine
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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Bryony Lynch
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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Mei Huang
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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Christopher G. DeSevo
3Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America
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Dave A. Pai
3Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America
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Cheryl M. Tucker
3Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America
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Margaret L. Hoang
4Howard Hughes Medical Institute and Department of Embryology, Carnegie Institution, Baltimore, Maryland, United States of America
5Department of Biology, Johns Hopkins University, Baltimore, Maryland, United States of America
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Maitreya J. Dunham
1Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
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  • For correspondence: maitreya@uw.edu
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Abstract

Evolutionary outcomes depend not only on the selective forces acting upon a species, but also on the genetic background. However, large timescales and uncertain historical selection pressures can make it difficult to discern such important background differences between species. Experimental evolution is one tool to compare evolutionary potential of known genotypes in a controlled environment. Here we utilized a highly reproducible evolutionary adaptation in Saccharomyces cerevisiae to investigate whether other yeast species would adopt similar evolutionary trajectories. We evolved populations of S. cerevisiae, S. paradoxus, S. mikatae, S. uvarum, and interspecific hybrids between S. uvarum and S. cerevisiae for ~200-500 generations in sulfate-limited continuous culture. Wild-type S. cerevisiae cultures invariably amplify the high affinity sulfate transporter gene, SUL1. However, while amplification of the SUL1 locus was detected in S. paradoxus and S. mikatae populations, S. uvarum cultures instead selected for amplification of the paralog, SUL2. We measured the relative fitness of strains bearing deletions and amplifications of both SUL genes from different species, confirming that, converse to S. cerevisiae, S. uvarum SUL2 contributes more to fitness in sulfate limitation than S. uvarum SUL1. By measuring the fitness and gene expression of chimeric promoter-ORF constructs, we were able to delineate the cause of this differential fitness effect primarily to the promoter of S. uvarum SUL1. Our data show evidence of differential sub-functionalization among the sulfur transporters across Saccharomyces species through recent changes in noncoding sequence. Furthermore, these results show a clear example of how such background differences due to paralog divergence can drive significant changes in evolutionary trajectories of eukaryotes.

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Posted July 12, 2016.
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Differential paralog divergence modulates evolutionary outcomes in yeast
Monica R. Sanchez, Aaron W. Miller, Ivan Liachko, Anna B. Sunshine, Bryony Lynch, Mei Huang, Christopher G. DeSevo, Dave A. Pai, Cheryl M. Tucker, Margaret L. Hoang, Maitreya J. Dunham
bioRxiv 063248; doi: https://doi.org/10.1101/063248
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Differential paralog divergence modulates evolutionary outcomes in yeast
Monica R. Sanchez, Aaron W. Miller, Ivan Liachko, Anna B. Sunshine, Bryony Lynch, Mei Huang, Christopher G. DeSevo, Dave A. Pai, Cheryl M. Tucker, Margaret L. Hoang, Maitreya J. Dunham
bioRxiv 063248; doi: https://doi.org/10.1101/063248

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