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The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection

Population adaptation to strong selection can occur through the sequential or parallel accumulation of competing beneficial mutations. The dynamics, diversity, and rate of fixation of beneficial mutations within and between populations are still poorly understood. To study how the mutational landsca...

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Autores principales: Payen, Celia, Di Rienzi, Sara C., Ong, Giang T., Pogachar, Jamie L., Sanchez, Joseph C., Sunshine, Anna B., Raghuraman, M. K., Brewer, Bonita J., Dunham, Maitreya J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3962480/
https://www.ncbi.nlm.nih.gov/pubmed/24368781
http://dx.doi.org/10.1534/g3.113.009365
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author Payen, Celia
Di Rienzi, Sara C.
Ong, Giang T.
Pogachar, Jamie L.
Sanchez, Joseph C.
Sunshine, Anna B.
Raghuraman, M. K.
Brewer, Bonita J.
Dunham, Maitreya J.
author_facet Payen, Celia
Di Rienzi, Sara C.
Ong, Giang T.
Pogachar, Jamie L.
Sanchez, Joseph C.
Sunshine, Anna B.
Raghuraman, M. K.
Brewer, Bonita J.
Dunham, Maitreya J.
author_sort Payen, Celia
collection PubMed
description Population adaptation to strong selection can occur through the sequential or parallel accumulation of competing beneficial mutations. The dynamics, diversity, and rate of fixation of beneficial mutations within and between populations are still poorly understood. To study how the mutational landscape varies across populations during adaptation, we performed experimental evolution on seven parallel populations of Saccharomyces cerevisiae continuously cultured in limiting sulfate medium. By combining quantitative polymerase chain reaction, array comparative genomic hybridization, restriction digestion and contour-clamped homogeneous electric field gel electrophoresis, and whole-genome sequencing, we followed the trajectory of evolution to determine the identity and fate of beneficial mutations. During a period of 200 generations, the yeast populations displayed parallel evolutionary dynamics that were driven by the coexistence of independent beneficial mutations. Selective amplifications rapidly evolved under this selection pressure, in particular common inverted amplifications containing the sulfate transporter gene SUL1. Compared with single clones, detailed analysis of the populations uncovers a greater complexity whereby multiple subpopulations arise and compete despite a strong selection. The most common evolutionary adaptation to strong selection in these populations grown in sulfate limitation is determined by clonal interference, with adaptive variants both persisting and replacing one another.
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spelling pubmed-39624802014-03-24 The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection Payen, Celia Di Rienzi, Sara C. Ong, Giang T. Pogachar, Jamie L. Sanchez, Joseph C. Sunshine, Anna B. Raghuraman, M. K. Brewer, Bonita J. Dunham, Maitreya J. G3 (Bethesda) Investigations Population adaptation to strong selection can occur through the sequential or parallel accumulation of competing beneficial mutations. The dynamics, diversity, and rate of fixation of beneficial mutations within and between populations are still poorly understood. To study how the mutational landscape varies across populations during adaptation, we performed experimental evolution on seven parallel populations of Saccharomyces cerevisiae continuously cultured in limiting sulfate medium. By combining quantitative polymerase chain reaction, array comparative genomic hybridization, restriction digestion and contour-clamped homogeneous electric field gel electrophoresis, and whole-genome sequencing, we followed the trajectory of evolution to determine the identity and fate of beneficial mutations. During a period of 200 generations, the yeast populations displayed parallel evolutionary dynamics that were driven by the coexistence of independent beneficial mutations. Selective amplifications rapidly evolved under this selection pressure, in particular common inverted amplifications containing the sulfate transporter gene SUL1. Compared with single clones, detailed analysis of the populations uncovers a greater complexity whereby multiple subpopulations arise and compete despite a strong selection. The most common evolutionary adaptation to strong selection in these populations grown in sulfate limitation is determined by clonal interference, with adaptive variants both persisting and replacing one another. Genetics Society of America 2013-12-24 /pmc/articles/PMC3962480/ /pubmed/24368781 http://dx.doi.org/10.1534/g3.113.009365 Text en Copyright © 2014 Payen et al.
spellingShingle Investigations
Payen, Celia
Di Rienzi, Sara C.
Ong, Giang T.
Pogachar, Jamie L.
Sanchez, Joseph C.
Sunshine, Anna B.
Raghuraman, M. K.
Brewer, Bonita J.
Dunham, Maitreya J.
The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title_full The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title_fullStr The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title_full_unstemmed The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title_short The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection
title_sort dynamics of diverse segmental amplifications in populations of saccharomyces cerevisiae adapting to strong selection
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3962480/
https://www.ncbi.nlm.nih.gov/pubmed/24368781
http://dx.doi.org/10.1534/g3.113.009365
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