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A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp

The linker histone H1 binds to the nucleosome core particle at the site where DNA enters and exits, and facilitates folding of the nucleosomes into a higher-order chromatin structure in eukaryotes. Additionally, some variant H1s promote specialized chromatin functions in cellular processes. Germline...

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Autores principales: Yuan, Bo, Yang, Yi, Yan, Zhichao, He, Chun, Sun, Yu H., Wang, Fei, Wang, Beibei, Shi, Jiamin, Xiao, Shan, Wang, Fang, Fang, Qi, Li, Fei, Ye, Xinhai, Ye, Gongyin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264595/
https://www.ncbi.nlm.nih.gov/pubmed/37325562
http://dx.doi.org/10.3389/fcell.2023.1166517
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author Yuan, Bo
Yang, Yi
Yan, Zhichao
He, Chun
Sun, Yu H.
Wang, Fei
Wang, Beibei
Shi, Jiamin
Xiao, Shan
Wang, Fang
Fang, Qi
Li, Fei
Ye, Xinhai
Ye, Gongyin
author_facet Yuan, Bo
Yang, Yi
Yan, Zhichao
He, Chun
Sun, Yu H.
Wang, Fei
Wang, Beibei
Shi, Jiamin
Xiao, Shan
Wang, Fang
Fang, Qi
Li, Fei
Ye, Xinhai
Ye, Gongyin
author_sort Yuan, Bo
collection PubMed
description The linker histone H1 binds to the nucleosome core particle at the site where DNA enters and exits, and facilitates folding of the nucleosomes into a higher-order chromatin structure in eukaryotes. Additionally, some variant H1s promote specialized chromatin functions in cellular processes. Germline-specific H1 variants have been reported in some model species with diverse roles in chromatin structure changes during gametogenesis. In insects, the current understanding of germline-specific H1 variants comes mainly from the studies in Drosophila melanogaster, and the information on this set of genes in other non-model insects remains largely unknown. Here, we identify two H1 variants (PpH1V1 and PpH1V2) that are specifically predominantly expressed in the testis of the parasitoid wasp Pteromalus puparum. Evolutionary analyses suggest that these H1 variant genes evolve rapidly, and are generally maintained as a single copy in Hymenoptera. Disruption of PpH1V1 function in the late larval stage male by RNA interference experiments has no phenotype on spermatogenesis in the pupal testis, but results in abnormal chromatin structure and low sperm fertility in the adult seminal vesicle. In addition, PpH1V2 knockdown has no detectable effect on spermatogenesis or male fertility. Collectively, our discovery indicates distinct functions of male germline-enriched H1 variants between parasitoid wasp Pteromalus and Drosophila, providing new insights into the role of insect H1 variants in gametogenesis. This study also highlights the functional complexity of germline-specific H1s in animals.
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spelling pubmed-102645952023-06-15 A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp Yuan, Bo Yang, Yi Yan, Zhichao He, Chun Sun, Yu H. Wang, Fei Wang, Beibei Shi, Jiamin Xiao, Shan Wang, Fang Fang, Qi Li, Fei Ye, Xinhai Ye, Gongyin Front Cell Dev Biol Cell and Developmental Biology The linker histone H1 binds to the nucleosome core particle at the site where DNA enters and exits, and facilitates folding of the nucleosomes into a higher-order chromatin structure in eukaryotes. Additionally, some variant H1s promote specialized chromatin functions in cellular processes. Germline-specific H1 variants have been reported in some model species with diverse roles in chromatin structure changes during gametogenesis. In insects, the current understanding of germline-specific H1 variants comes mainly from the studies in Drosophila melanogaster, and the information on this set of genes in other non-model insects remains largely unknown. Here, we identify two H1 variants (PpH1V1 and PpH1V2) that are specifically predominantly expressed in the testis of the parasitoid wasp Pteromalus puparum. Evolutionary analyses suggest that these H1 variant genes evolve rapidly, and are generally maintained as a single copy in Hymenoptera. Disruption of PpH1V1 function in the late larval stage male by RNA interference experiments has no phenotype on spermatogenesis in the pupal testis, but results in abnormal chromatin structure and low sperm fertility in the adult seminal vesicle. In addition, PpH1V2 knockdown has no detectable effect on spermatogenesis or male fertility. Collectively, our discovery indicates distinct functions of male germline-enriched H1 variants between parasitoid wasp Pteromalus and Drosophila, providing new insights into the role of insect H1 variants in gametogenesis. This study also highlights the functional complexity of germline-specific H1s in animals. Frontiers Media S.A. 2023-05-31 /pmc/articles/PMC10264595/ /pubmed/37325562 http://dx.doi.org/10.3389/fcell.2023.1166517 Text en Copyright © 2023 Yuan, Yang, Yan, He, Sun, Wang, Wang, Shi, Xiao, Wang, Fang, Li, Ye and Ye. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Yuan, Bo
Yang, Yi
Yan, Zhichao
He, Chun
Sun, Yu H.
Wang, Fei
Wang, Beibei
Shi, Jiamin
Xiao, Shan
Wang, Fang
Fang, Qi
Li, Fei
Ye, Xinhai
Ye, Gongyin
A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title_full A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title_fullStr A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title_full_unstemmed A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title_short A rapidly evolving single copy histone H1 variant is associated with male fertility in a parasitoid wasp
title_sort rapidly evolving single copy histone h1 variant is associated with male fertility in a parasitoid wasp
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264595/
https://www.ncbi.nlm.nih.gov/pubmed/37325562
http://dx.doi.org/10.3389/fcell.2023.1166517
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