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Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera

The heterochromatic genome compartment mediates strictly conserved cellular processes such as chromosome segregation, telomere integrity, and genome stability. Paradoxically, heterochromatic DNA sequence is wildly unconserved. Recent reports that many hybrid incompatibility genes encode heterochroma...

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Autores principales: Helleu, Quentin, Levine, Mia T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6188558/
https://www.ncbi.nlm.nih.gov/pubmed/29924345
http://dx.doi.org/10.1093/molbev/msy128
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author Helleu, Quentin
Levine, Mia T
author_facet Helleu, Quentin
Levine, Mia T
author_sort Helleu, Quentin
collection PubMed
description The heterochromatic genome compartment mediates strictly conserved cellular processes such as chromosome segregation, telomere integrity, and genome stability. Paradoxically, heterochromatic DNA sequence is wildly unconserved. Recent reports that many hybrid incompatibility genes encode heterochromatin proteins, together with the observation that interspecies hybrids suffer aberrant heterochromatin-dependent processes, suggest that heterochromatic DNA packaging requires species-specific innovations. Testing this model of coevolution between fast-evolving heterochromatic DNA and its packaging proteins begins with defining the latter. Here we describe many such candidates encoded by the Heterochromatin Protein 1 (HP1) gene family across Diptera, an insect Order that encompasses dramatic episodes of heterochromatic sequence turnover. Using BLAST, synteny analysis, and phylogenetic tree building across 64 Diptera genomes, we discovered a staggering 121 HP1 duplication events. In contrast, we observed virtually no gene duplication in gene families that share a common “chromodomain” with HP1s, including Polycomb and Su(var)3-9. The remarkably high number of Dipteran HP1 paralogs arises from distant clades undergoing convergent HP1 family amplifications. These independently derived, young HP1s span diverse ages, domain structures, and rates of molecular evolution, including episodes of positive selection. Moreover, independently derived HP1s exhibit convergent expression evolution. While ancient HP1 parent genes are transcribed ubiquitously, young HP1 paralogs are transcribed primarily in male germline tissue, a pattern typical of young genes. Pervasive gene youth, rapid evolution, and germline specialization implicate heterochromatin-encoded selfish elements driving recurrent HP1 gene family expansions. The 121 young genes offer valuable experimental traction for elucidating the germline processes shaped by Diptera’s many dramatic episodes of heterochromatin turnover.
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spelling pubmed-61885582018-10-22 Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera Helleu, Quentin Levine, Mia T Mol Biol Evol Discoveries The heterochromatic genome compartment mediates strictly conserved cellular processes such as chromosome segregation, telomere integrity, and genome stability. Paradoxically, heterochromatic DNA sequence is wildly unconserved. Recent reports that many hybrid incompatibility genes encode heterochromatin proteins, together with the observation that interspecies hybrids suffer aberrant heterochromatin-dependent processes, suggest that heterochromatic DNA packaging requires species-specific innovations. Testing this model of coevolution between fast-evolving heterochromatic DNA and its packaging proteins begins with defining the latter. Here we describe many such candidates encoded by the Heterochromatin Protein 1 (HP1) gene family across Diptera, an insect Order that encompasses dramatic episodes of heterochromatic sequence turnover. Using BLAST, synteny analysis, and phylogenetic tree building across 64 Diptera genomes, we discovered a staggering 121 HP1 duplication events. In contrast, we observed virtually no gene duplication in gene families that share a common “chromodomain” with HP1s, including Polycomb and Su(var)3-9. The remarkably high number of Dipteran HP1 paralogs arises from distant clades undergoing convergent HP1 family amplifications. These independently derived, young HP1s span diverse ages, domain structures, and rates of molecular evolution, including episodes of positive selection. Moreover, independently derived HP1s exhibit convergent expression evolution. While ancient HP1 parent genes are transcribed ubiquitously, young HP1 paralogs are transcribed primarily in male germline tissue, a pattern typical of young genes. Pervasive gene youth, rapid evolution, and germline specialization implicate heterochromatin-encoded selfish elements driving recurrent HP1 gene family expansions. The 121 young genes offer valuable experimental traction for elucidating the germline processes shaped by Diptera’s many dramatic episodes of heterochromatin turnover. Oxford University Press 2018-10 2018-06-19 /pmc/articles/PMC6188558/ /pubmed/29924345 http://dx.doi.org/10.1093/molbev/msy128 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Helleu, Quentin
Levine, Mia T
Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title_full Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title_fullStr Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title_full_unstemmed Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title_short Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera
title_sort recurrent amplification of the heterochromatin protein 1 (hp1) gene family across diptera
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6188558/
https://www.ncbi.nlm.nih.gov/pubmed/29924345
http://dx.doi.org/10.1093/molbev/msy128
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