A comparative transcriptomic study on developmental gonads provides novel insights into sex change in the protandrous black porgy (Acanthopagrus schlegelii)

Zhang, Kai; Xu, Jin; Zhang, Zhiwei; Huang, Yu; Ruan, Zhiqiang; Chen, Shuyin; Zhu, Fei; You, Xinxin; Jia, Chaofeng; Meng, Qian; Gu, Ruobo; Lin, Xin; Xu, Junmin; Xu, Pao; Zhang, Zhiyong; Shi, Qiong

doi:10.1016/j.ygeno.2018.11.006

Cited by 14 publications

(14 citation statements)

References 61 publications

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“…In black seabream, the sex switch is controlled by a series of male-related genes (dmrt1, piwi1, piwi2, sox9, sox30, and amh) and female-related genes (jnk1, vasa, wnt4, figla, and foxl2), most of which were involved in the signaling pathway of sex steroid hormones. The sex reversal is initiated by the decrease of male-related genes and the increase of female-related genes (Zhang et al, 2019). In yellowfin seabream, our results indicate that the sex reversal might be closely associated with 55 sex-related genes, most of which were involved in the signaling network of sex steroid hormones, such as estradiol and testosterone.…”

Section: The Mechanisms Of Natural Sex Reversal In Fish Speciesmentioning

confidence: 68%

“… Zhang et al (2019) report de novo transcriptome data of the gonads in black seabream, a fish species that has a close phylogenetic relationship with yellowfin seabream. The N50 length (2194 bp) and average length (1062 bp) are similar in these two species, whereas the number of assembled unigenes (71,765) in yellowfin seabream is less than that (109,504) in black seabream, suggesting that their genetic information is different.…”

Section: Discussionmentioning

confidence: 99%

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Gonadal Transcriptome Analysis of Sex-Related Genes in the Protandrous Yellowfin Seabream (Acanthopagrus latus)

Lin

Fang

et al. 2020

Front. Genet.

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Yellowfin seabream (Acanthopagrus latus), a protandrous hermaphroditic fish, is a good model for studying the mechanism of sex reversal. However, limited knowledge is known about the genetic information related to reproduction and sex differentiation in this species. Here, we performed de novo transcriptome sequencing analysis of the testis, ovotestis, and ovary to identify sex-related genes in yellowfin seabream. The results assembled 71,765 unigenes in which 16,126 and 17,560 unigenes were differentially expressed in the ovotestis and ovary compared to the testis, respectively. The most differentially expressed gene (DEG)-enriched Kyoto Encyclopedia of Genes and Genomes and GO pathways were closely associated with the synthesis of sex steroid hormones. Functional analyses identified 55 important sex-related DEGs, including 32 testis-biased DEGs (dmrt1, amh, and sox9, etc.), 20 ovary-biased DEGs (cyp19a, foxl2, and wnt4, etc.), and 3 ovotestis-biased DEGs (lhb, dmrt2, and foxh1). Furthermore, the testis-specific expression of dmrt1 and the brain-pituitary-ovary axis expression of foxl2 were characterized, suggesting that they might play important roles in sex differentiation in yellowfin seabream. Our present work provided an important molecular basis for elucidating the mechanisms underlying sexual transition and reproductional regulation in yellowfin seabream.

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Section: The Mechanisms Of Natural Sex Reversal In Fish Speciesmentioning

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Gonadal Transcriptome Analysis of Sex-Related Genes in the Protandrous Yellowfin Seabream (Acanthopagrus latus)

Lin

Fang

et al. 2020

Front. Genet.

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“…Recently, an increasing number of studies have been conducted to analyze the transcript properties of non-model fish species to shed light on the molecular regulatory mechanisms of sexual development. Significant differences in the global transcriptomic profiles of gonads have been detected between males and females, and sex-biased genes have been identified in both hermaphroditic species, such as Thalassoma bifasciatum [ 40 ] and Acanthopagrus schlegelii [ 41 ], and gonochoristic species, such as African cichlids [ 42 ] and Cynoglossus semilaevis [ 43 ]. However, almost no previous work has considered how social status affects the molecular networks of sexual development, which in turn regulate individual reproductive behavior, morphology, and physiology.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Profiling and Expression Localization of Key Sex-Related Genes in a Socially-Controlled Hermaphroditic Clownfish, Amphiprion clarkii

Wang

Tang

et al. 2022

IJMS

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Clownfish can be an excellent research model for investigating the socially-controlled sexual development of sequential hermaphrodite teleosts. However, the molecular cascades underlying the social cues that orchestrate the sexual development process remain poorly understood. Here, we performed a comparative transcriptomic analysis of gonads from females, males, and nonbreeders of Amphiprion clarkii, which constitute a complete social group, allowing us to investigate the molecular regulatory network under social control. Our analysis highlighted that the gonads of nonbreeders and males exhibited high similarities but were far from females, both in global transcriptomic profiles and histological characteristics, and identified numerous candidate genes involved in sexual development, some well-known and some novel. Significant upregulation of cyp19a1a, foxl2, nr5a1a, wnt4a, hsd3b7, and pgr in females provides strong evidence for the importance of steroidogenesis in ovarian development and maintenance, with cyp19a1a playing a central role. Amh and sox8 are two potential key factors that may regulate testicular tissue development in early and late stages, respectively, as they are expressed at higher levels in males than in females, but with slightly different expression timings. Unlike previous descriptions in other fishes, the unique expression pattern of dmrt1 in A. clarkii implied its potential function in both male and female gonads, and we speculated that it might play promoting roles in the early development of both testicular and ovarian tissues.

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“…To date, the molecular mechanism of sex change in several hermaphroditic fish has been studied through transcriptomic analysis. Based on these studies, a large number of DEGs were found between the different gonadal statuses, including the digonic species, such as 22,449 DEGs in the protandrous black porgy with a digonic gonad ( Zhang et al, 2019 ), 22,591 DEGs in the yellowfin seabream with a digonic gonad ( Acanthopagrus latus ) ( Li et al, 2020 ), 25,928 DEGs in the protogynous common pandora with a digonic gonad ( Pagellus erythrinus ) ( Tsakogiannis et al, 2018 ), 18,724 DEGs in the juvenile bisexually red porgy with a digonic gonad ( Pagrus ) ( Tsakogiannis et al, 2018 ), and syngonic species, such as 5,483 DEGs in the protogynous clownfish with a syngonic gonad ( Amphiprion bicinctus ) ( Casas et al, 2016 ) and 20,183 DEGs in the protogynous bluehead wrasse ( Thalassoma bifasciatum ) ( Liu et al, 2015 ). These positive results (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…In a previous study, the transcriptomes of some hermaphroditic fish were also evaluated to identify the sex determination genes. A previous transcriptomic study on black porgy gonads provided several candidate genes ( jnk1 , vasa , wnt4 , figla , and foxl2 ) that are associated with secondary sex determination and differentiation ( Zhang et al, 2019 ). The steroidogenesis-related genes (such as hsd17b1 , hsd11b3 , hsd17b12 , and cyp19a1a ), androgen/estrogen receptor genes (such as ara , arb , and erb ), Wnt/beta-catenin signaling genes (such as wnt4a , wnt9b , ctnnb1 , and fst ), and female-related genes (such as foxl2 , gdf9 , bmp15 , gsdf , and sox3 ) are considered to involve female sex fate in yellowfin seabream ( Li et al, 2020 ), bluehead wrasses ( Liu et al, 2015 ), ricefield eel ( Cai et al, 2017 ), common pandora ( Tsakogiannis et al, 2018 ), and red porgy ( Tsakogiannis et al, 2018 ) ( Supplementary Table S2 ).…”

Section: Discussionmentioning

confidence: 99%

The Ovarian Transcriptome at the Early Stage of Testis Removal-Induced Male-To-Female Sex Change in the Protandrous Black Porgy Acanthopagrus schlegelii

Tseng

Kuo

et al. 2022

Front. Genet.

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Unlike gonochoristic fishes, sex is fixed after gonadal differentiation (primary sex determination), and sex can be altered in adults (secondary sex determination) of hermaphroditic fish species. The secondary sex determination of hermaphroditic fish has focused on the differences between testicular tissue and ovarian tissue during the sex change process. However, comprehensive studies analyzing ovarian tissue or testicular tissue independently have not been performed. Hermaphroditic black porgy shows a digonic gonad (ovarian tissue with testicular tissue separated by connective tissue). Protandrous black porgy has stable maleness during the first two reproductive cycles (<2 years old), and approximately 50% enter femaleness (natural sex change) during the third reproductive cycle. Precocious femaleness is rarely observed in the estradiol-17β (E2)-induced female phase (oocytes maintained at the primary oocyte stage), and a reversible female-to-male sex change is found after E2 is withdrawn in <2-year-old fish. However, precocious femaleness (oocytes entering the vitellogenic oocyte stage) is observed in testis-removed fish in <2-year-old fish. We used this characteristic to study secondary sex determination (femaleness) in ovarian tissue via transcriptomic analysis. Cell proliferation analysis showed that BrdU (5-bromo-2′-deoxyuridine)-incorporated germline cells were significantly increased in the testis-removed fish (female) compared to the control (sham) fish (male) during the nonspawning season (2 months after surgery). qPCR analysis showed that there were no differences in pituitary-releasing hormones (lhb and gtha) in pituitary and ovarian steroidogenesis-related factors (star, cyp11a1, hsd3b1, and cyp19a1a) or female-related genes (wnt4a, bmp15, gdf9, figla, and foxl2) in ovarian tissues between intact and testis-removed fish (2 months after surgery). Low expression of pituitary fshb and ovarian cyp17a1 was found after 2 months of surgery. However, we did find small numbers of genes (289 genes) showing sexual fate dimorphic expression in both groups by transcriptomic analysis (1 month after surgery). The expression profiles of these differentially expressed genes were further examined by qPCR. Our present work identified several candidate genes in ovarian tissue that may be involved in the early period of secondary sex determination (femaleness) in black porgy. The data confirmed our previous suggestion that testicular tissue plays an important role in secondary sex determination in protandrous black porgy.

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A comparative transcriptomic study on developmental gonads provides novel insights into sex change in the protandrous black porgy (Acanthopagrus schlegelii)

Cited by 14 publications

References 61 publications

Gonadal Transcriptome Analysis of Sex-Related Genes in the Protandrous Yellowfin Seabream (Acanthopagrus latus)

Gonadal Transcriptome Analysis of Sex-Related Genes in the Protandrous Yellowfin Seabream (Acanthopagrus latus)

Transcriptome Profiling and Expression Localization of Key Sex-Related Genes in a Socially-Controlled Hermaphroditic Clownfish, Amphiprion clarkii

The Ovarian Transcriptome at the Early Stage of Testis Removal-Induced Male-To-Female Sex Change in the Protandrous Black Porgy Acanthopagrus schlegelii

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