Differential paralog divergence modulates genome evolution across yeast species.
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 evoluti...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2017-02-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC5308817?pdf=render |
| _version_ | 1819113452642238464 |
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| author | Monica R Sanchez Aaron W Miller Ivan Liachko Anna B Sunshine Bryony Lynch Mei Huang Erica Alcantara Christopher G DeSevo Dave A Pai Cheryl M Tucker Margaret L Hoang Maitreya J Dunham |
| author_facet | Monica R Sanchez Aaron W Miller Ivan Liachko Anna B Sunshine Bryony Lynch Mei Huang Erica Alcantara Christopher G DeSevo Dave A Pai Cheryl M Tucker Margaret L Hoang Maitreya J Dunham |
| author_sort | Monica R Sanchez |
| collection | DOAJ |
| description | 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 experimental evolution of other yeast species would select for similar adaptive mutations. 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 sulfate 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 changes in genome evolution. |
| first_indexed | 2024-12-22T04:29:38Z |
| format | Article |
| id | doaj.art-99b13bdbe9b3403c95f09013dfc3ba3d |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-22T04:29:38Z |
| publishDate | 2017-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-99b13bdbe9b3403c95f09013dfc3ba3d2022-12-21T18:39:04ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-02-01132e100658510.1371/journal.pgen.1006585Differential paralog divergence modulates genome evolution across yeast species.Monica R SanchezAaron W MillerIvan LiachkoAnna B SunshineBryony LynchMei HuangErica AlcantaraChristopher G DeSevoDave A PaiCheryl M TuckerMargaret L HoangMaitreya J DunhamEvolutionary 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 experimental evolution of other yeast species would select for similar adaptive mutations. 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 sulfate 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 changes in genome evolution.http://europepmc.org/articles/PMC5308817?pdf=render |
| spellingShingle | Monica R Sanchez Aaron W Miller Ivan Liachko Anna B Sunshine Bryony Lynch Mei Huang Erica Alcantara Christopher G DeSevo Dave A Pai Cheryl M Tucker Margaret L Hoang Maitreya J Dunham Differential paralog divergence modulates genome evolution across yeast species. PLoS Genetics |
| title | Differential paralog divergence modulates genome evolution across yeast species. |
| title_full | Differential paralog divergence modulates genome evolution across yeast species. |
| title_fullStr | Differential paralog divergence modulates genome evolution across yeast species. |
| title_full_unstemmed | Differential paralog divergence modulates genome evolution across yeast species. |
| title_short | Differential paralog divergence modulates genome evolution across yeast species. |
| title_sort | differential paralog divergence modulates genome evolution across yeast species |
| url | http://europepmc.org/articles/PMC5308817?pdf=render |
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