Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals

Background: Although the mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes. The surviving genes are a specialized set with extraordinary evolutionary longevity. Mos...

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Main Authors: Hughes, Jennifer F, Skaletsky, Helen, Koutseva, Natalia, Pyntikova, Tatyana, Page, David C
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Published: Biomed Central Ltd 2018
Online Access:http://hdl.handle.net/1721.1/116788
https://orcid.org/0000-0001-9920-3411
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author Hughes, Jennifer F
Skaletsky, Helen
Koutseva, Natalia
Pyntikova, Tatyana
Page, David C
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Hughes, Jennifer F
Skaletsky, Helen
Koutseva, Natalia
Pyntikova, Tatyana
Page, David C
author_sort Hughes, Jennifer F
collection MIT
description Background: Although the mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes. The surviving genes are a specialized set with extraordinary evolutionary longevity. Most mammalian lineages have experienced delayed, or relatively recent, loss of at least one conserved Y-linked gene. An extreme example of this phenomenon is in the Japanese spiny rat, where the Y chromosome has disappeared altogether. In this species, many Y-linked genes were rescued by transposition to new genomic locations, but until our work presented here, this has been considered an isolated case. Results: We describe eight cases of genes that have relocated to autosomes in mammalian lineages where the corresponding Y-linked gene has been lost. These gene transpositions originated from either the X or Y chromosomes, and are observed in diverse mammalian lineages: occurring at least once in marsupials, apes, and cattle, and at least twice in rodents and marmoset. For two genes - EIF1AX/Y and RPS4X/Y - transposition to autosomes occurred independently in three distinct lineages. Conclusions: Rescue of Y-linked gene loss through transposition to autosomes has previously been reported for a single isolated rodent species. However, our findings indicate that this compensatory mechanism is widespread among mammalian species. Thus, Y-linked gene loss emerges as an additional driver of gene transposition from the sex chromosomes, a phenomenon thought to be driven primarily by meiotic sex chromosome inactivation.
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spelling mit-1721.1/1167882022-10-02T05:12:53Z Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals Hughes, Jennifer F Skaletsky, Helen Koutseva, Natalia Pyntikova, Tatyana Page, David C Massachusetts Institute of Technology. Department of Biology Page, David C Background: Although the mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes. The surviving genes are a specialized set with extraordinary evolutionary longevity. Most mammalian lineages have experienced delayed, or relatively recent, loss of at least one conserved Y-linked gene. An extreme example of this phenomenon is in the Japanese spiny rat, where the Y chromosome has disappeared altogether. In this species, many Y-linked genes were rescued by transposition to new genomic locations, but until our work presented here, this has been considered an isolated case. Results: We describe eight cases of genes that have relocated to autosomes in mammalian lineages where the corresponding Y-linked gene has been lost. These gene transpositions originated from either the X or Y chromosomes, and are observed in diverse mammalian lineages: occurring at least once in marsupials, apes, and cattle, and at least twice in rodents and marmoset. For two genes - EIF1AX/Y and RPS4X/Y - transposition to autosomes occurred independently in three distinct lineages. Conclusions: Rescue of Y-linked gene loss through transposition to autosomes has previously been reported for a single isolated rodent species. However, our findings indicate that this compensatory mechanism is widespread among mammalian species. Thus, Y-linked gene loss emerges as an additional driver of gene transposition from the sex chromosomes, a phenomenon thought to be driven primarily by meiotic sex chromosome inactivation. National Institutes of Health (U.S.) (Grant HG000257) 2018-07-05T14:10:24Z 2018-07-05T14:10:24Z 2015-05 2015-02 2018-07-02T14:25:48Z Article http://purl.org/eprint/type/JournalArticle 1474-760X http://hdl.handle.net/1721.1/116788 Hughes, Jennifer F et al “Sex Chromosome-to-Autosome Transposition Events Counter Y-Chromosome Gene Loss in Mammals.” Genome Biology 16, 1 (May 2015): 104 © 2015 Hughes et al https://orcid.org/0000-0001-9920-3411 http://dx.doi.org/10.1186/S13059-015-0667-4 Genome Biology Creative Commons Attribution 4.0 International License http://creativecommons.org/licenses/by/4.0/ application/pdf Biomed Central Ltd BioMedCentral
spellingShingle Hughes, Jennifer F
Skaletsky, Helen
Koutseva, Natalia
Pyntikova, Tatyana
Page, David C
Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title_full Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title_fullStr Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title_full_unstemmed Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title_short Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals
title_sort sex chromosome to autosome transposition events counter y chromosome gene loss in mammals
url http://hdl.handle.net/1721.1/116788
https://orcid.org/0000-0001-9920-3411
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