Sex determination mechanisms and sex control approaches in aquaculture animals

Li, Xi-Yin; Mei, Jie; Ge, Chutian; Liu, Xiaoli; Gui, Jian‐Fang

doi:10.1007/s11427-021-2075-x

Cited by 82 publications

(36 citation statements)

References 391 publications

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“…Additionally, we failed to obtain any informative male-specific supernumerary sequences from one male individual of C. gibelio (Supplementary Note 7). A high-quality male genome assembly for C. gibelio will be required to uncover the mechanisms underlying male determination 62 and gene conversion in the future.…”

Section: Discussionmentioning

confidence: 99%

Comparative genome anatomy reveals evolutionary insights into a unique amphitriploid fish

Wang

et al. 2022

Nat Ecol Evol

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Triploids are rare in nature because of difficulties in meiotic and gametogenic processes, especially in vertebrates. The Carassius complex of cyprinid teleosts contains sexual tetraploid crucian carp/goldfish (C. auratus) and unisexual hexaploid gibel carp/Prussian carp (C. gibelio) lineages, providing a valuable model for studying the evolution and maintenance mechanism of unisexual polyploids in vertebrates. Here we sequence the genomes of the two species and assemble their haplotypes, which contain two subgenomes (A and B), to the chromosome level. Sequencing coverage analysis reveals that C. gibelio is an amphitriploid (AAABBB) with two triploid sets of chromosomes; each set is derived from a different ancestor. Resequencing data from different strains of C. gibelio show that unisexual reproduction has been maintained for over 0.82 million years. Comparative genomics show intensive expansion and alterations of meiotic cell cycle-related genes and an oocyte-specific histone variant. Cytological assays indicate that C. gibelio produces unreduced oocytes by an alternative ameiotic pathway; however, sporadic homologous recombination and a high rate of gene conversion also exist in C. gibelio. These genomic changes might have facilitated purging deleterious mutations and maintaining genome stability in this unisexual amphitriploid fish. Overall, the current results provide novel insights into the evolutionary mechanisms of the reproductive success in unisexual polyploid vertebrates.

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Section: Discussionmentioning

confidence: 99%

Comparative genome anatomy reveals evolutionary insights into a unique amphitriploid fish

Wang

et al. 2022

Nat Ecol Evol

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“…The origin and maintenance of unisexual vertebrates have long fascinated evolutionary biologists, and unisexual animals are considered ideal systems for addressing some long-standing and fundamental questions in ecology and evolution ( Gui and Zhou 2010 ; Van de Peer et al 2017 ; Brunes et al 2019 ; Laskowski et al 2019 ; Gui et al 2022 ; Li et al 2022 ). Over 100 species or biotypes across around 22 genera of fish, amphibians, and reptiles are able to reproduce via parthenogenesis, gynogenesis, or hybridogenesis ( Gui and Zhou 2010 ; Avise 2015 ; Zhou and Gui 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Zhu

et al. 2022

Molecular Biology and Evolution

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Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian carp or goldfish) (AABB) and the gynogenetic amphitriploid C. gibelio (gibel carp) (AAABBB). Recently, we developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome. In this study, we generated novel amphitriploids (AAABBB) by backcrossing the amphitetraploid male with the amphidiploid C. auratus. Whole-genome resequencing revealed the genomic changes, including recombination and independent assortment between homologs of C. gibelio and C. auratus. The fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids were investigated. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte (with and without homolog synapsis) were discovered, and their distinct development fates were observed. Type I oocytes entered apoptosis due to improper synaptonemal complex assembly and incomplete double-strand break repair, whereas subsequent type II oocytes bypassed meiosis through an alternative ameiotic pathway to develop into mature eggs. Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced. These revealed genomic changes and detailed cytological data provide comprehensive evidence that changes in ploidy drive unisexual and sexual reproduction transition, thereby resulting in genomic diversity and allowing C. gibelio avoid genomic decay.

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“…In sharp contrast to the remarkable diversity of sex-determining switches [36][37][38], the downstream genetic cascades of sex differentiation are relatively conserved [37,[39][40][41]. Members of the transforming growth factor-β (TGF-β) signaling pathway have been identified as being vastly involved in sex determination and differentiation in vertebrates [36,42].…”

Section: Introductionmentioning

confidence: 99%

Two duplicated gsdf homeologs cooperatively regulate male differentiation by inhibiting cyp19a1a transcription in a hexaploid fish

Wang

Ding

et al. 2022

PLoS Genet

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Although evolutionary fates and expression patterns of duplicated genes have been extensively investigated, how duplicated genes co-regulate a biological process in polyploids remains largely unknown. Here, we identified two gsdf (gonadal somatic cell-derived factor) homeologous genes (gsdf-A and gsdf-B) in hexaploid gibel carp (Carassius gibelio), wherein each homeolog contained three highly conserved alleles. Interestingly, gsdf-A and gsdf-B transcription were mainly activated by dmrt1-A (dsx- and mab-3-related transcription factor 1) and dmrt1-B, respectively. Loss of either gsdf-A or gsdf-B alone resulted in partial male-to-female sex reversal and loss of both caused complete sex reversal, which could be rescued by a nonsteroidal aromatase inhibitor. Compensatory expression of gsdf-A and gsdf-B was observed in gsdf-B and gsdf-A mutants, respectively. Subsequently, we determined that in tissue culture cells, Gsdf-A and Gsdf-B both interacted with Ncoa5 (nuclear receptor coactivator 5) and blocked Ncoa5 interaction with Rora (retinoic acid-related orphan receptor-alpha) to repress Rora/Ncoa5-induced activation of cyp19a1a (cytochrome P450, family 19, subfamily A, polypeptide 1a). These findings illustrate that Gsdf-A and Gsdf-B can regulate male differentiation by inhibiting cyp19a1a transcription in hexaploid gibel carp and also reveal that Gsdf-A and Gsdf-B can interact with Ncoa5 to suppress cyp19a1a transcription in vitro. This study provides a typical case of cooperative mechanism of duplicated genes in polyploids and also sheds light on the conserved evolution of sex differentiation.

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Sex determination mechanisms and sex control approaches in aquaculture animals

Cited by 82 publications

References 391 publications

Comparative genome anatomy reveals evolutionary insights into a unique amphitriploid fish

Comparative genome anatomy reveals evolutionary insights into a unique amphitriploid fish

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Two duplicated gsdf homeologs cooperatively regulate male differentiation by inhibiting cyp19a1a transcription in a hexaploid fish

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