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Transposable Element Mobilization in Interspecific Yeast Hybrids

Barbara McClintock first hypothesized that interspecific hybridization could provide a “genomic shock” that leads to the mobilization of transposable elements (TEs). This hypothesis is based on the idea that regulation of TE movement is potentially disrupted in hybrids. However, the handful of studi...

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Autores principales: Smukowski Heil, Caiti, Patterson, Kira, Hickey, Angela Shang-Mei, Alcantara, Erica, Dunham, Maitreya J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952228/
https://www.ncbi.nlm.nih.gov/pubmed/33595639
http://dx.doi.org/10.1093/gbe/evab033
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author Smukowski Heil, Caiti
Patterson, Kira
Hickey, Angela Shang-Mei
Alcantara, Erica
Dunham, Maitreya J
author_facet Smukowski Heil, Caiti
Patterson, Kira
Hickey, Angela Shang-Mei
Alcantara, Erica
Dunham, Maitreya J
author_sort Smukowski Heil, Caiti
collection PubMed
description Barbara McClintock first hypothesized that interspecific hybridization could provide a “genomic shock” that leads to the mobilization of transposable elements (TEs). This hypothesis is based on the idea that regulation of TE movement is potentially disrupted in hybrids. However, the handful of studies testing this hypothesis have yielded mixed results. Here, we set out to identify if hybridization can increase transposition rate and facilitate colonization of TEs in Saccharomyces cerevisiae × Saccharomyces uvarum interspecific yeast hybrids. Saccharomyces cerevisiae have a small number of active long terminal repeat retrotransposons (Ty elements), whereas their distant relative S. uvarum have lost the Ty elements active in S. cerevisiae. Although the regulation system of Ty elements is known in S. cerevisiae, it is unclear how Ty elements are regulated in other Saccharomyces species, and what mechanisms contributed to the loss of most classes of Ty elements in S. uvarum. Therefore, we first assessed whether TEs could insert in the S. uvarum sub-genome of a S. cerevisiae × S. uvarum hybrid. We induced transposition to occur in these hybrids and developed a sequencing technique to show that Ty elements insert readily and nonrandomly in the S. uvarum genome. We then used an in vivo reporter construct to directly measure transposition rate in hybrids, demonstrating that hybridization itself does not alter rate of mobilization. However, we surprisingly show that species-specific mitochondrial inheritance can change transposition rate by an order of magnitude. Overall, our results provide evidence that hybridization can potentially facilitate the introduction of TEs across species boundaries and alter transposition via mitochondrial transmission, but that this does not lead to unrestrained proliferation of TEs suggested by the genomic shock theory.
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spelling pubmed-79522282021-03-16 Transposable Element Mobilization in Interspecific Yeast Hybrids Smukowski Heil, Caiti Patterson, Kira Hickey, Angela Shang-Mei Alcantara, Erica Dunham, Maitreya J Genome Biol Evol Research Article Barbara McClintock first hypothesized that interspecific hybridization could provide a “genomic shock” that leads to the mobilization of transposable elements (TEs). This hypothesis is based on the idea that regulation of TE movement is potentially disrupted in hybrids. However, the handful of studies testing this hypothesis have yielded mixed results. Here, we set out to identify if hybridization can increase transposition rate and facilitate colonization of TEs in Saccharomyces cerevisiae × Saccharomyces uvarum interspecific yeast hybrids. Saccharomyces cerevisiae have a small number of active long terminal repeat retrotransposons (Ty elements), whereas their distant relative S. uvarum have lost the Ty elements active in S. cerevisiae. Although the regulation system of Ty elements is known in S. cerevisiae, it is unclear how Ty elements are regulated in other Saccharomyces species, and what mechanisms contributed to the loss of most classes of Ty elements in S. uvarum. Therefore, we first assessed whether TEs could insert in the S. uvarum sub-genome of a S. cerevisiae × S. uvarum hybrid. We induced transposition to occur in these hybrids and developed a sequencing technique to show that Ty elements insert readily and nonrandomly in the S. uvarum genome. We then used an in vivo reporter construct to directly measure transposition rate in hybrids, demonstrating that hybridization itself does not alter rate of mobilization. However, we surprisingly show that species-specific mitochondrial inheritance can change transposition rate by an order of magnitude. Overall, our results provide evidence that hybridization can potentially facilitate the introduction of TEs across species boundaries and alter transposition via mitochondrial transmission, but that this does not lead to unrestrained proliferation of TEs suggested by the genomic shock theory. Oxford University Press 2021-02-17 /pmc/articles/PMC7952228/ /pubmed/33595639 http://dx.doi.org/10.1093/gbe/evab033 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Smukowski Heil, Caiti
Patterson, Kira
Hickey, Angela Shang-Mei
Alcantara, Erica
Dunham, Maitreya J
Transposable Element Mobilization in Interspecific Yeast Hybrids
title Transposable Element Mobilization in Interspecific Yeast Hybrids
title_full Transposable Element Mobilization in Interspecific Yeast Hybrids
title_fullStr Transposable Element Mobilization in Interspecific Yeast Hybrids
title_full_unstemmed Transposable Element Mobilization in Interspecific Yeast Hybrids
title_short Transposable Element Mobilization in Interspecific Yeast Hybrids
title_sort transposable element mobilization in interspecific yeast hybrids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952228/
https://www.ncbi.nlm.nih.gov/pubmed/33595639
http://dx.doi.org/10.1093/gbe/evab033
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