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

BMC Genomics, Nov 2015

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.

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

Liu et al. BMC Genomics Complete depletion of primordial germ cells in an All-female fish leads to Sex- biased gene expression alteration and sterile All-male occurrence Wei Liu 0 Shi-Zhu Li 0 Zhi Li Yang Wang Xi-Yin Li Jian-Xiang Zhong Xiao-Juan Zhang Jun Zhang Li Zhou Jian-Fang Gui 0 Equal contributors State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Graduate University of the Chinese Academy of Sciences , Wuhan 430072 , China 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. Sexual dimorphism; Gonad differentiation; Primordial germ cells; Gynogenesis; Sex-biased gene; Carassius gibelio Background Primordial germ cells (PGCs), the ancestors of sperms and eggs, arise before the formation of gonadal somatic cells and migrate to genital ridge, in which the PGCs and somatic cells form primordial gonad [ 1, 2 ]. Then, the primordial gonad differentiates into a testis or an ovary under their collaboration [3]. In mammals, the sexual fate is determined by a Y-linked Sry gene, which initiates a cascade of events to trigger the primordial gonads to differentiate into testes [ 4 ]. And, the Sry expression in common precursors also triggers differentiation of the somatic precursors into Sertoli cells [ 5 ]. In Japanese medaka, a Y-specific Dmy, which is expressed in the gonadal somatic cells of XY embryos, has been revealed to make the gonads differentiate into testes [ 6 ]. Moreover, several sex determination-related or sex chromosomelinked genes have been identified, and most of them are the duplications of dmrt1 (dsx and mab-3 related transcription factor 1) [ 7–10 ]. As primordial gonad is composed of PGCs and somatic precursors, and gonadal differentiation and gametogenesis must go through a long and complicated developmental process, the interaction between germ cells and somatic cells is therefore very critical for the process completion [11]. In mammals, the germ cell-depleted XY mouse embryos were not found to affect the ability of supporting cells to develop into testicular cords [ 12 ], whereas in XX mouse, germ cell ablation before birth did not affect the ovary development [ 13 ]. Moreover, through losing sex determination-related gene dmrt1 in mature testis or by depleting female determination-related gene foxl2 in mature ovary, the gonadal somatic cell sex was also demonstrated to be required for testis or ovary maintenance throughout adulthood [ 14, 15 ]. More complicated roles of germ cells on gonad differentiation and sexual dimorphism had been observed in teleost fish and reptilian turtle. In Japanese medaka, Kurokawa et al. [16] revealed that loss of germ cells in XX medaka resulted in a failure to maintain female supporting cells and the somatic cells acquired male supporting cell characteristics, in which the produced androgens made the germ cell-depleted medaka undergo a female-to-male sex reversal in secondary sex characteristics. In zebrafish, the germ cell-depleted fish were demonstrated to be males, and the oocytes were confirmed to be required for a stable maintenance of sexual phenotype in adults [ 17–19 ]. Moreover, the number of germ cells was also demonstrated to contribute to sex differentiation and gonad dimorphism in zebrafish and medaka, in which the embryos with a number of germ cells lower than a threshold develop into males, while those with plenty of germ cells becom (...truncated)


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Wei Liu, Shi-Zhu Li, Zhi Li, Yang Wang, Xi-Yin Li, Jian-Xiang Zhong, Xiao-Juan Zhang, Jun Zhang, Li Zhou, Jian-Fang Gui. Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence, BMC Genomics, 2015, pp. 971, 16, DOI: 10.1186/s12864-015-2130-z