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Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits

Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploi...

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Autores principales: Naseeb, Samina, Visinoni, Federico, Hu, Yue, Hinks Roberts, Alex J., Maslowska, Agnieszka, Walsh, Thomas, Smart, Katherine A., Louis, Edward J., Delneri, Daniela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8463882/
https://www.ncbi.nlm.nih.gov/pubmed/34518218
http://dx.doi.org/10.1073/pnas.2101242118
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author Naseeb, Samina
Visinoni, Federico
Hu, Yue
Hinks Roberts, Alex J.
Maslowska, Agnieszka
Walsh, Thomas
Smart, Katherine A.
Louis, Edward J.
Delneri, Daniela
author_facet Naseeb, Samina
Visinoni, Federico
Hu, Yue
Hinks Roberts, Alex J.
Maslowska, Agnieszka
Walsh, Thomas
Smart, Katherine A.
Louis, Edward J.
Delneri, Daniela
author_sort Naseeb, Samina
collection PubMed
description Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and –independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.
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spelling pubmed-84638822021-10-27 Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits Naseeb, Samina Visinoni, Federico Hu, Yue Hinks Roberts, Alex J. Maslowska, Agnieszka Walsh, Thomas Smart, Katherine A. Louis, Edward J. Delneri, Daniela Proc Natl Acad Sci U S A Biological Sciences Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and –independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity. National Academy of Sciences 2021-09-21 2021-09-13 /pmc/articles/PMC8463882/ /pubmed/34518218 http://dx.doi.org/10.1073/pnas.2101242118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Naseeb, Samina
Visinoni, Federico
Hu, Yue
Hinks Roberts, Alex J.
Maslowska, Agnieszka
Walsh, Thomas
Smart, Katherine A.
Louis, Edward J.
Delneri, Daniela
Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title_full Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title_fullStr Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title_full_unstemmed Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title_short Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
title_sort restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8463882/
https://www.ncbi.nlm.nih.gov/pubmed/34518218
http://dx.doi.org/10.1073/pnas.2101242118
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