Cargando…

Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence

BACKGROUND: Gynogenesis is one of unisexual reproduction modes in vertebrates, and produces all-female individuals with identical genetic background. In sexual reproduction vertebrates, the roles of primordial germ cells on sexual dimorphism and gonadal differentiation have been largely studied, and...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Wei, Li, Shi-Zhu, Li, Zhi, Wang, Yang, Li, Xi-Yin, Zhong, Jian-Xiang, Zhang, Xiao-Juan, Zhang, Jun, Zhou, Li, Gui, Jian-Fang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4652418/
https://www.ncbi.nlm.nih.gov/pubmed/26582363
http://dx.doi.org/10.1186/s12864-015-2130-z
_version_ 1782401750481764352
author Liu, Wei
Li, Shi-Zhu
Li, Zhi
Wang, Yang
Li, Xi-Yin
Zhong, Jian-Xiang
Zhang, Xiao-Juan
Zhang, Jun
Zhou, Li
Gui, Jian-Fang
author_facet Liu, Wei
Li, Shi-Zhu
Li, Zhi
Wang, Yang
Li, Xi-Yin
Zhong, Jian-Xiang
Zhang, Xiao-Juan
Zhang, Jun
Zhou, Li
Gui, Jian-Fang
author_sort Liu, Wei
collection PubMed
description BACKGROUND: Gynogenesis is one of unisexual reproduction modes in vertebrates, and produces all-female individuals with identical genetic background. In sexual reproduction vertebrates, the roles of primordial germ cells on sexual dimorphism and gonadal differentiation have been largely studied, and two distinct functional models have been proposed. However, the role of primordial germ cells remains unknown in unisexual animals, and it is also unclear whether the functional models in sexual reproduction animals are common in unisexual animals. RESULTS: To solve these puzzles, we attempt to utilize the gynogenetic superiority of polyploid Carassius gibelio to create a complete germ cell-depleted gonad model by a similar morpholino-mediated knockdown approach used in other examined sexual reproduction fishes. Through the germ cell-depleted gonad model, we have performed comprehensive and comparative transcriptome analysis, and revealed a complete alteration of sex-biased gene expression. Moreover, the expression alteration leads to up-regulation of testis-biased genes and down-regulation of ovary-biased genes, and results in the occurrence of sterile all-males with testis-like gonads and secondary sex characteristics in the germ cell-depleted gynogenetic Carassius gibelio. CONCLUSIONS: Our current results have demonstrated that unisexual gynogenetic embryos remain keeping male sex determination information in the genome, and the complete depletion of primordial germ cells in the all-female fish leads to sex-biased gene expression alteration and sterile all-male occurrence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2130-z) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4652418
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-46524182015-11-20 Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence Liu, Wei Li, Shi-Zhu Li, Zhi Wang, Yang Li, Xi-Yin Zhong, Jian-Xiang Zhang, Xiao-Juan Zhang, Jun Zhou, Li Gui, Jian-Fang BMC Genomics Research Article BACKGROUND: Gynogenesis is one of unisexual reproduction modes in vertebrates, and produces all-female individuals with identical genetic background. In sexual reproduction vertebrates, the roles of primordial germ cells on sexual dimorphism and gonadal differentiation have been largely studied, and two distinct functional models have been proposed. However, the role of primordial germ cells remains unknown in unisexual animals, and it is also unclear whether the functional models in sexual reproduction animals are common in unisexual animals. RESULTS: To solve these puzzles, we attempt to utilize the gynogenetic superiority of polyploid Carassius gibelio to create a complete germ cell-depleted gonad model by a similar morpholino-mediated knockdown approach used in other examined sexual reproduction fishes. Through the germ cell-depleted gonad model, we have performed comprehensive and comparative transcriptome analysis, and revealed a complete alteration of sex-biased gene expression. Moreover, the expression alteration leads to up-regulation of testis-biased genes and down-regulation of ovary-biased genes, and results in the occurrence of sterile all-males with testis-like gonads and secondary sex characteristics in the germ cell-depleted gynogenetic Carassius gibelio. CONCLUSIONS: Our current results have demonstrated that unisexual gynogenetic embryos remain keeping male sex determination information in the genome, and the complete depletion of primordial germ cells in the all-female fish leads to sex-biased gene expression alteration and sterile all-male occurrence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2130-z) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-18 /pmc/articles/PMC4652418/ /pubmed/26582363 http://dx.doi.org/10.1186/s12864-015-2130-z Text en © Liu et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Liu, Wei
Li, Shi-Zhu
Li, Zhi
Wang, Yang
Li, Xi-Yin
Zhong, Jian-Xiang
Zhang, Xiao-Juan
Zhang, Jun
Zhou, Li
Gui, Jian-Fang
Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title_full Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title_fullStr Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title_full_unstemmed Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title_short Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence
title_sort complete depletion of primordial germ cells in an all-female fish leads to sex-biased gene expression alteration and sterile all-male occurrence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4652418/
https://www.ncbi.nlm.nih.gov/pubmed/26582363
http://dx.doi.org/10.1186/s12864-015-2130-z
work_keys_str_mv AT liuwei completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT lishizhu completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT lizhi completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT wangyang completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT lixiyin completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT zhongjianxiang completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT zhangxiaojuan completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT zhangjun completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT zhouli completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence
AT guijianfang completedepletionofprimordialgermcellsinanallfemalefishleadstosexbiasedgeneexpressionalterationandsterileallmaleoccurrence