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Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution
Mammalian X and Y Chromosomes evolved from an ordinary autosomal pair. Genetic decay of the Y led to X Chromosome inactivation (XCI) in females, but some Y-linked genes were retained during the course of sex chromosome evolution, and many X-linked genes did not become subject to XCI. We reconstructe...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory Press
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880238/ https://www.ncbi.nlm.nih.gov/pubmed/29449410 http://dx.doi.org/10.1101/gr.230433.117 |
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author | Naqvi, Sahin Bellott, Daniel W. Lin, Kathy S. Page, David C. |
author_facet | Naqvi, Sahin Bellott, Daniel W. Lin, Kathy S. Page, David C. |
author_sort | Naqvi, Sahin |
collection | PubMed |
description | Mammalian X and Y Chromosomes evolved from an ordinary autosomal pair. Genetic decay of the Y led to X Chromosome inactivation (XCI) in females, but some Y-linked genes were retained during the course of sex chromosome evolution, and many X-linked genes did not become subject to XCI. We reconstructed gene-by-gene dosage sensitivities on the ancestral autosomes through phylogenetic analysis of microRNA (miRNA) target sites and compared these preexisting characteristics to the current status of Y-linked and X-linked genes in mammals. Preexisting heterogeneities in dosage sensitivity, manifesting as differences in the extent of miRNA-mediated repression, predicted either the retention of a Y homolog or the acquisition of XCI following Y gene decay. Analogous heterogeneities among avian Z-linked genes predicted either the retention of a W homolog or gene-specific dosage compensation following W gene decay. Genome-wide analyses of human copy number variation indicate that these heterogeneities consisted of sensitivity to both increases and decreases in dosage. We propose a model of XY/ZW evolution incorporating such preexisting dosage sensitivities in determining the evolutionary fates of individual genes. Our findings thus provide a more complete view of the role of dosage sensitivity in shaping the mammalian and avian sex chromosomes and reveal an important role for post-transcriptional regulatory sequences (miRNA target sites) in sex chromosome evolution. |
format | Online Article Text |
id | pubmed-5880238 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-58802382018-04-13 Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution Naqvi, Sahin Bellott, Daniel W. Lin, Kathy S. Page, David C. Genome Res Research Mammalian X and Y Chromosomes evolved from an ordinary autosomal pair. Genetic decay of the Y led to X Chromosome inactivation (XCI) in females, but some Y-linked genes were retained during the course of sex chromosome evolution, and many X-linked genes did not become subject to XCI. We reconstructed gene-by-gene dosage sensitivities on the ancestral autosomes through phylogenetic analysis of microRNA (miRNA) target sites and compared these preexisting characteristics to the current status of Y-linked and X-linked genes in mammals. Preexisting heterogeneities in dosage sensitivity, manifesting as differences in the extent of miRNA-mediated repression, predicted either the retention of a Y homolog or the acquisition of XCI following Y gene decay. Analogous heterogeneities among avian Z-linked genes predicted either the retention of a W homolog or gene-specific dosage compensation following W gene decay. Genome-wide analyses of human copy number variation indicate that these heterogeneities consisted of sensitivity to both increases and decreases in dosage. We propose a model of XY/ZW evolution incorporating such preexisting dosage sensitivities in determining the evolutionary fates of individual genes. Our findings thus provide a more complete view of the role of dosage sensitivity in shaping the mammalian and avian sex chromosomes and reveal an important role for post-transcriptional regulatory sequences (miRNA target sites) in sex chromosome evolution. Cold Spring Harbor Laboratory Press 2018-04 /pmc/articles/PMC5880238/ /pubmed/29449410 http://dx.doi.org/10.1101/gr.230433.117 Text en © 2018 Naqvi et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Research Naqvi, Sahin Bellott, Daniel W. Lin, Kathy S. Page, David C. Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title | Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title_full | Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title_fullStr | Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title_full_unstemmed | Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title_short | Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
title_sort | conserved microrna targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880238/ https://www.ncbi.nlm.nih.gov/pubmed/29449410 http://dx.doi.org/10.1101/gr.230433.117 |
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