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)