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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Biomed Central Ltd
2018
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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. |
first_indexed | 2024-09-23T15:56:20Z |
format | Article |
id | mit-1721.1/116788 |
institution | Massachusetts Institute of Technology |
last_indexed | 2024-09-23T15:56:20Z |
publishDate | 2018 |
publisher | Biomed Central Ltd |
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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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