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Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function

Sex-specific traits that lead to the production of dimorphic gametes, sperm in males and eggs in females, are fundamental for sexual reproduction and accordingly widespread among animals. Yet the sex-biased genes that underlie these sex-specific traits are under strong selective pressure, and as a r...

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Autores principales: Shah, Chirag, VanGompel, Michael J. W., Naeem, Villian, Chen, Yanmei, Lee, Terrance, Angeloni, Nicholas, Wang, Yin, Xu, Eugene Yujun
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2904765/
https://www.ncbi.nlm.nih.gov/pubmed/20657660
http://dx.doi.org/10.1371/journal.pgen.1001022
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author Shah, Chirag
VanGompel, Michael J. W.
Naeem, Villian
Chen, Yanmei
Lee, Terrance
Angeloni, Nicholas
Wang, Yin
Xu, Eugene Yujun
author_facet Shah, Chirag
VanGompel, Michael J. W.
Naeem, Villian
Chen, Yanmei
Lee, Terrance
Angeloni, Nicholas
Wang, Yin
Xu, Eugene Yujun
author_sort Shah, Chirag
collection PubMed
description Sex-specific traits that lead to the production of dimorphic gametes, sperm in males and eggs in females, are fundamental for sexual reproduction and accordingly widespread among animals. Yet the sex-biased genes that underlie these sex-specific traits are under strong selective pressure, and as a result of adaptive evolution they often become divergent. Indeed out of hundreds of male or female fertility genes identified in diverse organisms, only a very small number of them are implicated specifically in reproduction in more than one lineage. Few genes have exhibited a sex-biased, reproductive-specific requirement beyond a given phylum, raising the question of whether any sex-specific gametogenesis factors could be conserved and whether gametogenesis might have evolved multiple times. Here we describe a metazoan origin of a conserved human reproductive protein, BOULE, and its prevalence from primitive basal metazoans to chordates. We found that BOULE homologs are present in the genomes of representative species of each of the major lineages of metazoans and exhibit reproductive-specific expression in all species examined, with a preponderance of male-biased expression. Examination of Boule evolution within insect and mammalian lineages revealed little evidence for accelerated evolution, unlike most reproductive genes. Instead, purifying selection was the major force behind Boule evolution. Furthermore, loss of function of mammalian Boule resulted in male-specific infertility and a global arrest of sperm development remarkably similar to the phenotype in an insect boule mutation. This work demonstrates the conservation of a reproductive protein throughout eumetazoa, its predominant testis-biased expression in diverse bilaterian species, and conservation of a male gametogenic requirement in mice. This shows an ancient gametogenesis requirement for Boule among Bilateria and supports a model of a common origin of spermatogenesis.
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spelling pubmed-29047652010-07-23 Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function Shah, Chirag VanGompel, Michael J. W. Naeem, Villian Chen, Yanmei Lee, Terrance Angeloni, Nicholas Wang, Yin Xu, Eugene Yujun PLoS Genet Research Article Sex-specific traits that lead to the production of dimorphic gametes, sperm in males and eggs in females, are fundamental for sexual reproduction and accordingly widespread among animals. Yet the sex-biased genes that underlie these sex-specific traits are under strong selective pressure, and as a result of adaptive evolution they often become divergent. Indeed out of hundreds of male or female fertility genes identified in diverse organisms, only a very small number of them are implicated specifically in reproduction in more than one lineage. Few genes have exhibited a sex-biased, reproductive-specific requirement beyond a given phylum, raising the question of whether any sex-specific gametogenesis factors could be conserved and whether gametogenesis might have evolved multiple times. Here we describe a metazoan origin of a conserved human reproductive protein, BOULE, and its prevalence from primitive basal metazoans to chordates. We found that BOULE homologs are present in the genomes of representative species of each of the major lineages of metazoans and exhibit reproductive-specific expression in all species examined, with a preponderance of male-biased expression. Examination of Boule evolution within insect and mammalian lineages revealed little evidence for accelerated evolution, unlike most reproductive genes. Instead, purifying selection was the major force behind Boule evolution. Furthermore, loss of function of mammalian Boule resulted in male-specific infertility and a global arrest of sperm development remarkably similar to the phenotype in an insect boule mutation. This work demonstrates the conservation of a reproductive protein throughout eumetazoa, its predominant testis-biased expression in diverse bilaterian species, and conservation of a male gametogenic requirement in mice. This shows an ancient gametogenesis requirement for Boule among Bilateria and supports a model of a common origin of spermatogenesis. Public Library of Science 2010-07-15 /pmc/articles/PMC2904765/ /pubmed/20657660 http://dx.doi.org/10.1371/journal.pgen.1001022 Text en Shah et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Shah, Chirag
VanGompel, Michael J. W.
Naeem, Villian
Chen, Yanmei
Lee, Terrance
Angeloni, Nicholas
Wang, Yin
Xu, Eugene Yujun
Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title_full Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title_fullStr Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title_full_unstemmed Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title_short Widespread Presence of Human BOULE Homologs among Animals and Conservation of Their Ancient Reproductive Function
title_sort widespread presence of human boule homologs among animals and conservation of their ancient reproductive function
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2904765/
https://www.ncbi.nlm.nih.gov/pubmed/20657660
http://dx.doi.org/10.1371/journal.pgen.1001022
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