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Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep

BACKGROUND: The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked regi...

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Autores principales: VanBuren, Robert, Wai, Ching Man, Zhang, Jisen, Han, Jennifer, Arro, Jie, Lin, Zhicong, Liao, Zhenyang, Yu, Qingyi, Wang, Ming-Li, Zee, Francis, Moore, Richard C., Charlesworth, Deborah, Ming, Ray
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5125041/
https://www.ncbi.nlm.nih.gov/pubmed/27890017
http://dx.doi.org/10.1186/s13059-016-1095-9
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author VanBuren, Robert
Wai, Ching Man
Zhang, Jisen
Han, Jennifer
Arro, Jie
Lin, Zhicong
Liao, Zhenyang
Yu, Qingyi
Wang, Ming-Li
Zee, Francis
Moore, Richard C.
Charlesworth, Deborah
Ming, Ray
author_facet VanBuren, Robert
Wai, Ching Man
Zhang, Jisen
Han, Jennifer
Arro, Jie
Lin, Zhicong
Liao, Zhenyang
Yu, Qingyi
Wang, Ming-Li
Zee, Francis
Moore, Richard C.
Charlesworth, Deborah
Ming, Ray
author_sort VanBuren, Robert
collection PubMed
description BACKGROUND: The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked region. RESULTS: Diversity is very low for all genes in the X-linked region in the wild dioecious population, with nucleotide diversity π (syn) = 0.00017, tenfold lower than the autosomal region (π (syn) = 0.0017) and 12-fold lower than the Y-linked region (π (syn) = 0.0021). Analysis of the X-linked sequences shows an undivided population, suggesting a geographically wide diversity-reducing event, whereas two subpopulations were observed in the autosomes separating gynodioecy and dioecy and three subpopulations in the Y-linked region separating three male populations. The extremely low diversity in the papaya X-linked region was probably caused by a recent, strong selective sweep before domestication, involving either the spread of a recessive mutation in an X-linked gene that is beneficial to males or a partially dominant mutation that benefitted females or both sexes. Nucleotide diversity in the domesticated X samples is about half that in the wild Xs, probably due to the bottleneck when hermaphrodites were selected during domestication. CONCLUSIONS: The extreme low nucleotide diversity in the papaya X-linked region is much greater than observed in humans, great apes, and the neo-X chromosome of Drosophila miranda, which show the expected pattern of Y-linked genes < X-linked genes < autosomal genes; papaya shows an unprecedented pattern of X-linked genes < autosomal genes < Y-linked genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-1095-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-51250412016-12-08 Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep VanBuren, Robert Wai, Ching Man Zhang, Jisen Han, Jennifer Arro, Jie Lin, Zhicong Liao, Zhenyang Yu, Qingyi Wang, Ming-Li Zee, Francis Moore, Richard C. Charlesworth, Deborah Ming, Ray Genome Biol Research BACKGROUND: The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked region. RESULTS: Diversity is very low for all genes in the X-linked region in the wild dioecious population, with nucleotide diversity π (syn) = 0.00017, tenfold lower than the autosomal region (π (syn) = 0.0017) and 12-fold lower than the Y-linked region (π (syn) = 0.0021). Analysis of the X-linked sequences shows an undivided population, suggesting a geographically wide diversity-reducing event, whereas two subpopulations were observed in the autosomes separating gynodioecy and dioecy and three subpopulations in the Y-linked region separating three male populations. The extremely low diversity in the papaya X-linked region was probably caused by a recent, strong selective sweep before domestication, involving either the spread of a recessive mutation in an X-linked gene that is beneficial to males or a partially dominant mutation that benefitted females or both sexes. Nucleotide diversity in the domesticated X samples is about half that in the wild Xs, probably due to the bottleneck when hermaphrodites were selected during domestication. CONCLUSIONS: The extreme low nucleotide diversity in the papaya X-linked region is much greater than observed in humans, great apes, and the neo-X chromosome of Drosophila miranda, which show the expected pattern of Y-linked genes < X-linked genes < autosomal genes; papaya shows an unprecedented pattern of X-linked genes < autosomal genes < Y-linked genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-1095-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-28 /pmc/articles/PMC5125041/ /pubmed/27890017 http://dx.doi.org/10.1186/s13059-016-1095-9 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
VanBuren, Robert
Wai, Ching Man
Zhang, Jisen
Han, Jennifer
Arro, Jie
Lin, Zhicong
Liao, Zhenyang
Yu, Qingyi
Wang, Ming-Li
Zee, Francis
Moore, Richard C.
Charlesworth, Deborah
Ming, Ray
Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title_full Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title_fullStr Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title_full_unstemmed Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title_short Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep
title_sort extremely low nucleotide diversity in the x-linked region of papaya caused by a strong selective sweep
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5125041/
https://www.ncbi.nlm.nih.gov/pubmed/27890017
http://dx.doi.org/10.1186/s13059-016-1095-9
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