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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...

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Detalles Bibliográficos
Autores principales: Naqvi, Sahin, Bellott, Daniel W., Lin, Kathy S., Page, David C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
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.
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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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