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Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve

BACKGROUND: Interspecific hybridization occurs in every eukaryotic kingdom. While hybrid progeny are frequently at a selective disadvantage, in some instances their increased genome size and complexity may result in greater stress resistance than their ancestors, which can be adaptively advantageous...

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Autores principales: Piotrowski, Jeff S, Nagarajan, Saisubramanian, Kroll, Evgueny, Stanbery, Alison, Chiotti, Kami E, Kruckeberg, Arthur L, Dunn, Barbara, Sherlock, Gavin, Rosenzweig, Frank
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3372441/
https://www.ncbi.nlm.nih.gov/pubmed/22471618
http://dx.doi.org/10.1186/1471-2148-12-46
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author Piotrowski, Jeff S
Nagarajan, Saisubramanian
Kroll, Evgueny
Stanbery, Alison
Chiotti, Kami E
Kruckeberg, Arthur L
Dunn, Barbara
Sherlock, Gavin
Rosenzweig, Frank
author_facet Piotrowski, Jeff S
Nagarajan, Saisubramanian
Kroll, Evgueny
Stanbery, Alison
Chiotti, Kami E
Kruckeberg, Arthur L
Dunn, Barbara
Sherlock, Gavin
Rosenzweig, Frank
author_sort Piotrowski, Jeff S
collection PubMed
description BACKGROUND: Interspecific hybridization occurs in every eukaryotic kingdom. While hybrid progeny are frequently at a selective disadvantage, in some instances their increased genome size and complexity may result in greater stress resistance than their ancestors, which can be adaptively advantageous at the edges of their ancestors' ranges. While this phenomenon has been repeatedly documented in the field, the response of hybrid populations to long-term selection has not often been explored in the lab. To fill this knowledge gap we crossed the two most distantly related members of the Saccharomyces sensu stricto group, S. cerevisiae and S. uvarum, and established a mixed population of homoploid and aneuploid hybrids to study how different types of selection impact hybrid genome structure. RESULTS: As temperature was raised incrementally from 31°C to 46.5°C over 500 generations of continuous culture, selection favored loss of the S. uvarum genome, although the kinetics of genome loss differed among independent replicates. Temperature-selected isolates exhibited greater inherent and induced thermal tolerance than parental species and founding hybrids, and also exhibited ethanol resistance. In contrast, as exogenous ethanol was increased from 0% to 14% over 500 generations of continuous culture, selection favored euploid S. cerevisiae x S. uvarum hybrids. Ethanol-selected isolates were more ethanol tolerant than S. uvarum and one of the founding hybrids, but did not exhibit resistance to temperature stress. Relative to parental and founding hybrids, temperature-selected strains showed heritable differences in cell wall structure in the forms of increased resistance to zymolyase digestion and Micafungin, which targets cell wall biosynthesis. CONCLUSIONS: This is the first study to show experimentally that the genomic fate of newly-formed interspecific hybrids depends on the type of selection they encounter during the course of evolution, underscoring the importance of the ecological theatre in determining the outcome of the evolutionary play.
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spelling pubmed-33724412012-06-12 Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve Piotrowski, Jeff S Nagarajan, Saisubramanian Kroll, Evgueny Stanbery, Alison Chiotti, Kami E Kruckeberg, Arthur L Dunn, Barbara Sherlock, Gavin Rosenzweig, Frank BMC Evol Biol Research Article BACKGROUND: Interspecific hybridization occurs in every eukaryotic kingdom. While hybrid progeny are frequently at a selective disadvantage, in some instances their increased genome size and complexity may result in greater stress resistance than their ancestors, which can be adaptively advantageous at the edges of their ancestors' ranges. While this phenomenon has been repeatedly documented in the field, the response of hybrid populations to long-term selection has not often been explored in the lab. To fill this knowledge gap we crossed the two most distantly related members of the Saccharomyces sensu stricto group, S. cerevisiae and S. uvarum, and established a mixed population of homoploid and aneuploid hybrids to study how different types of selection impact hybrid genome structure. RESULTS: As temperature was raised incrementally from 31°C to 46.5°C over 500 generations of continuous culture, selection favored loss of the S. uvarum genome, although the kinetics of genome loss differed among independent replicates. Temperature-selected isolates exhibited greater inherent and induced thermal tolerance than parental species and founding hybrids, and also exhibited ethanol resistance. In contrast, as exogenous ethanol was increased from 0% to 14% over 500 generations of continuous culture, selection favored euploid S. cerevisiae x S. uvarum hybrids. Ethanol-selected isolates were more ethanol tolerant than S. uvarum and one of the founding hybrids, but did not exhibit resistance to temperature stress. Relative to parental and founding hybrids, temperature-selected strains showed heritable differences in cell wall structure in the forms of increased resistance to zymolyase digestion and Micafungin, which targets cell wall biosynthesis. CONCLUSIONS: This is the first study to show experimentally that the genomic fate of newly-formed interspecific hybrids depends on the type of selection they encounter during the course of evolution, underscoring the importance of the ecological theatre in determining the outcome of the evolutionary play. BioMed Central 2012-04-02 /pmc/articles/PMC3372441/ /pubmed/22471618 http://dx.doi.org/10.1186/1471-2148-12-46 Text en Copyright ©2012 Piotrowski et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Piotrowski, Jeff S
Nagarajan, Saisubramanian
Kroll, Evgueny
Stanbery, Alison
Chiotti, Kami E
Kruckeberg, Arthur L
Dunn, Barbara
Sherlock, Gavin
Rosenzweig, Frank
Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title_full Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title_fullStr Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title_full_unstemmed Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title_short Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
title_sort different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3372441/
https://www.ncbi.nlm.nih.gov/pubmed/22471618
http://dx.doi.org/10.1186/1471-2148-12-46
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