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Published on: March 7, 2019
A Genetic Incompatibility Accelerates Adaptation in Yeast
Duyen T Bui1, Elliot Dine1, James B Anderson2
1Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, United States of America.
Abstract:
During mismatch repair (MMR) MSH proteins bind to mismatches that form as the result of DNA replication errors and recruit MLH factors such as Mlh1-Pms1 to initiate excision and repair steps. Previously, we identified a negative epistatic interaction involving naturally occurring polymorphisms in the MLH1 and PMS1 genes of baker's yeast. Here we hypothesize that a mutagenic state resulting from this negative epistatic interaction increases the likelihood of obtaining beneficial mutations that can promote adaptation to stress conditions. We tested this by stressing yeast strains bearing mutagenic (incompatible) and non-mutagenic (compatible) mismatch repair genotypes. Our data show that incompatible populations adapted more rapidly and without an apparent fitness cost to high salt stress. The fitness advantage of incompatible populations was rapid but disappeared over time. The fitness gains in both compatible and incompatible strains were due primarily to mutations in PMR1 that appeared earlier in incompatible evolving populations. These data demonstrate a rapid and reversible role (by mating) for genetic incompatibilities in accelerating adaptation in eukaryotes. They also provide an approach to link experimental studies to observational population genomics.
Insights
Genetic incompatibilities in DNA mismatch repair (MMR) accelerate adaptation to stress by increasing beneficial mutations. This effect is rapid, reversible, and linked to specific gene mutations, offering insights into eukaryotic evolution.
Area of Science:
- Evolutionary Biology
- Genetics
- Molecular Biology
Background:
- DNA mismatch repair (MMR) corrects replication errors using MSH and MLH proteins.
- Naturally occurring polymorphisms in MLH1 and PMS1 genes in yeast exhibit negative epistasis.
- This genetic interaction creates a mutagenic state with potential adaptive advantages.
Purpose of the Study:
- To test the hypothesis that a mutagenic MMR state accelerates adaptation to stress conditions.
- To investigate the role of genetic incompatibilities in promoting beneficial mutations.
- To link experimental findings to observational population genomics.
Main Methods:
- Yeast strains with mutagenic (incompatible) and non-mutagenic (compatible) MMR genotypes were stressed.
- Adaptation rates and fitness costs under high salt stress were measured.
- Genomic analysis identified mutations responsible for fitness gains, focusing on PMR1.
Main Results:
- Incompatible yeast populations adapted more rapidly to high salt stress without immediate fitness cost.
- This fitness advantage was transient, disappearing over time.
- Adaptation in both compatible and incompatible strains was primarily driven by mutations in PMR1, appearing earlier in incompatible populations.
Conclusions:
- Genetic incompatibilities within the MMR system can rapidly accelerate adaptation in eukaryotes.
- The adaptive advantage conferred by these incompatibilities is reversible through mating.
- This study provides a framework for connecting experimental evolution with population genomics.
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