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Characterization of Early Gonadal Differentiation and Induction of Sex Reversal in the Rock Bream Oplegnathus fasciatus

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Abstract

Rock bream (Oplegnathus fasciatus) is a typical fish that has a unique multiple sex chromosome system (♀X1X1X2X2/♂X1X2Y). We examined the early gonadal development in rock bream via continuous histological observations of the gonads at 40–120 days post hatching (dph). The fish was identified as a typical gonochorist, and female gonads were found to differentiate earlier than male gonads. The ovarian cavity of the female was initially observed at 80 dph, whereas the efferent duct of the male was not observed until 100 dph. Immunofluorescence with the vasa-antibody revealed that germ cells were predominantly distributed around the ovarian cavity in females and on the edge of the gonad in males during the early stages of sex differentiation. Sex reversal was induced via the oral administration of letrozole (LTZ), 17α-methyltestosterone (MT), and 17β-estradiol (E2), respectively, during the labile period of gonadal development. LTZ and MT induced 100% masculinization of genotype-females, whereas E2 induced only 50–60% feminization of genotype-males. Such findings suggest that the fish retained high sexual plasticity despite the existence of the neo-Y chromosome. MT and E2 had negative effect on fish growth, whereas LTZ did not exert such side effect. LTZ and MT could accelerate gonadal development in sex-reversed genotype-males, whereas E2 inhibited gonadal development in genotype-females of rock bream. These findings provide a basis for further research on the mechanisms of sex determination and differentiation in fishes with X1X2Y sex chromosome system and provide a sex reversal protocol for rock bream.

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References

  • Babiak J, Babiak I, Nes SV, Harboe T, Haugen T, Norberg B (2012) Induced sex reversal using an aromatase inhibitor, fadrozole, in Atlantic halibut (Hippoglossus L.). Aquaculture 324:276–280

    Article  Google Scholar 

  • Bem JC, Fontanetti CS, Senhorini JA, Parise-Maltempi PP (2012) Effectiveness of estradiol valerate on sex reversion in Astyanax altiparanae (Characiformes, Characidae). Braz Arch Biol Technol 55:283–290

    Article  Google Scholar 

  • Budd AM, Banh QQ, Domingos JA, Jerry DR (2015) Sex control in fish: approaches, challenges and opportunities for aquaculture. J Mar Sci Eng 3:329–355

    Article  Google Scholar 

  • Carvalho CV, Passini G, Costa WM, Cerqueira VR (2014) Feminization and growth of juvenile fat snook Centropomus parallelus fed diets with different concentrations of 17β-estradiol. Aquaculture 22:1391–1401

    Google Scholar 

  • Chi M, Jia Y, Cheng S, Liu S, Jiang W, Zheng J, Gu Z (2019) Effects of 17α-methyltestosterone on the growth performance, development, and reproduction of gynogenetic topmouth culter (Culter alburnus Basilewsky). J Appl Ichthyol 35:444–456

    Article  CAS  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • El-Greisy ZA, El-Gamal AE (2012) Monosex production of tilapia, Oreochromis niloticus using different doses of 17α-methyltestosterone with respect to the degree of sex stability after one year of treatment. Egypt J Aquat Res 38:59–66

    Article  Google Scholar 

  • Filby AL, Thorpe KL, Maack G, Tyler CR (2007) Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquat Toxicol 81:219–231

    Article  CAS  PubMed  Google Scholar 

  • Filby AL, Thorpe KL, Tyler CR (2006) Multiple molecular effect pathways of an environmental oestrogen in fish. J Mol Endocrinol 37:121–134

    Article  CAS  PubMed  Google Scholar 

  • Flynn SR, Benfey TJ (2007) Effects of dietary 17β-estradiol in juvenile shortnose sturgeon, Acipenser brevirostrum, Lesueur. Aquaculture 270:405–412

    Article  CAS  Google Scholar 

  • Gao Z, Wang HP, Rapp D, O’Bryant P, Wallat G, Wang W, Yao H, Tiu L, MacDonald R (2009) Gonadal sex differentiation in the bluegill sunfish Lepomis macrochirus and its relation to fish size and age. Aquaculture 294:138–146

    Article  Google Scholar 

  • Gong J, Li B, Zhao J, Zhou Z, Ke Q, Zhu Q, Xu D, Zhou T, Xu P (2022) Sex-specific genomic region identification and molecular sex marker development of rock bream (Oplegnathus fasciatus). Mar Biotechnol 24:163–173

    Article  CAS  Google Scholar 

  • Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352–366

    Article  CAS  PubMed  Google Scholar 

  • Haugen T, Andersson E, Norberg B, Taranger GL (2011) The production of hermaphrodites of Atlantic cod (Gadus morhua) by masculinization with orally administered 17α-methyltestosterone, and subsequent production of all-female cod populations. Aquaculture 311:248–254

    Article  CAS  Google Scholar 

  • Kang X, Ning j, Mu S, Li F, Su W, Liu X, (2010) Histological studies of early embryonic gonadal anlage differentiation of Cynoglossus semilaevis. J Hebei Univ 30:296–300

    Google Scholar 

  • Karki NP, Colombo RE, Gaines KF, Maia A (2021) Exposure to 17β-estradiol causes erosion of sexual dimorphism in bluegill (Lepomis macrochirus). Environ Sci Pollut Res Int 28:6450–6458

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y, Nagahama Y, Nakamura M (2013) Diversity and plasticity of sex determination and differentiation in fishes. Sex Dev 7:115–125

    Article  CAS  PubMed  Google Scholar 

  • Komen J, De-Boer P, Richter JJ (1992) Male sex reversal in gynogentic XX females of common carp (Cyprinus carpio L) by a recessive mutation in a sex-determining gene. J Hered 83:431–434

    Article  Google Scholar 

  • Li H, Zhu Q, Chen R, Liu M, Xu D (2021a) Identification and characterization of dimorphic expression of sex-related genes in rock bream, a fish with multiple sex chromosomes. Front Genet 12:791179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Zhang R, Fan G, Xu W, Zhou Q, Wang L, Li W, Pang Z, Yu M, Liu Q, Liu X, Schartl M, Chen S (2021b) Reconstruction of the origin of a neo-Y sex chromosome and its evolution in the spotted knifejaw, Oplegnathus punctatus. Mol Biol Evol 38:2615–2626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XY, Mei J, Ge CT, Liu XL, Gui JF (2022) Sex determination mechanisms and sex control approaches in aquaculture animals. Sci China Life Sci 65:1091–1122

    Article  PubMed  Google Scholar 

  • Lin S, Benfey TJ, Martin-Robichaud DJ (2012) Hormonal sex reversal in Atlantic cod, Gadus morhua. Aquaculture 364:192–197

    Article  Google Scholar 

  • Luckenbach JA, Fairgrieve WT, Hayman ES (2017) Establishment of monosex female production of sablefish (Anoplopoma fimbria) through direct and indirect sex control. Aquaculture 479:285–296

    Article  CAS  Google Scholar 

  • Ma S, Gen Z, Xu D, Lou B, Mao G, Zhang W (2014) Histological observations on the gonadal development of Nibea albiflora. J Zhejiang Ocean Univ 33:129–133

    Google Scholar 

  • Nakamura M (2013) Morphological and physiological studies on gonadal sex differentiation in teleost fish. Aqua-Biosci Monogr 6:1–47

    Article  Google Scholar 

  • Nishimura T, Tanaka M (2014) Gonadal development in fish. Sex Dev 8:252–261

    Article  PubMed  Google Scholar 

  • Pandian TJ, Sheela SG (1995) Hormonal induction of sex reversal in fish. Aquaculture 138:1–22

    Article  CAS  Google Scholar 

  • Patrick S, Bodilis P, Evans J, Francour P (2010) Occurrence of barred knifejaw, Oplegnathus Fasciatus (Actinopterygii: Perciformes: Oplegnathidae), in malta (Central Mediterranean) with a discussion on possible modes of entry. Acta Ichthyol Piscat 40:101–104

    Article  Google Scholar 

  • Pereira TSB, Boscolo CNP, Batlouni S (2020) Use of 17β-estradiol for Leporinus macrocephalus feminization. Bol Inst Pesca 46:1–7

    Article  Google Scholar 

  • Qin Z, Yang F, Tian L, Chen R, Xu D, Takeuchi Y (2020) Induction of sex reversal in blue drum (Nibea mitsukurii) and gynogenetic yellow drum (Nibea albiflora) by oral administration of letrozole. Aquac Res 51:882–889

    Article  CAS  Google Scholar 

  • Riley LG, Richman NH, Hirano T, Grau EG (2002) Activation of the growth hormone/insulin-like growth factor axis by treatment with 17α-methyltestosterone and seawater rearing in the tilapia, Oreochromis mossambicus. Genl Comp Endocr 127:285–292

    Article  CAS  Google Scholar 

  • Shen ZG, Fan QX, Yang W, Zhang YL, Wang HP (2015) Effects of 17α-methyltestosterone and aromatase inhibitor letrozole on sex reversal, gonadal structure, and growth in yellow catfish Pelteobagrus fulvidraco. Biol Bull 228:108–117

    Article  CAS  PubMed  Google Scholar 

  • Teal CN, Schill DJ, Fogelson SB, Roberts CM, Fitzsimmons K, Bauder JM, Stewart WT, Bonar SA (2023) The effects of 17β-estradiol on the sex reversal, survival, and growth of green sunfish Lepomis cyanellus. Aquaculture 562:738853

    Article  CAS  Google Scholar 

  • Vidal-López JM, Contreras-Sánchez WM, Contreras-García AHMJ, Uribe-Aranzábal MC (2019) Functional feminization of the Mexican snook (Centropomus poeyi) using 17β-estradiol in the diet. Lat Am J Aquat Res 47:240–250

    Article  Google Scholar 

  • Xiao Y, Xiao Z, Ma D, Liu J, Li J (2019) Genome sequence of the barred knifejaw Oplegnathus fasciatus (Temminck & Schlegel, 1844): the first chromosome-level draft genome in the family Oplegnathidae. Gigascience 8:giz013.

  • Xiao Y, Xiao Z, Ma D, Zhao C, Liu L, Wu H, Nie W, Xiao S, Liu J, Li J, Herrera-Ulloa A (2020) Chromosome-level genome reveals the origin of neo-Y chromosome in the male barred knifejaw Oplegnathus fasciatus. iScience 23:101039.

  • Xie B, Xiong S, Mei J (2017) Identification and expression of gengs related to sex determination and differentiation in Peltobagrus fulvidraco. Hubei Agricult Sci 56:2362–2367

    Google Scholar 

  • Xie QP, Li BB, Wei FL, Yu M, Zhan W, Liu F, Lou B (2021) Growth and gonadal development retardations after long-term exposure to estradiol in little yellow croaker. Larimichthys Polyactis Ecotoxicol Environ Saf 222:112462

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Lou B, Bertollo LA, Cioffi MDB (2013) Chromosomal mapping of microsatellite repeats in the rock bream fish Oplegnathus fasciatus, with emphasis of their distribution in the neo-Y chromosome. Mol Cytogenet 6:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Sember A, Zhu Q, Oliveira ED, Liehr T, Al-Rikabi ABH, Xiao Z, Song H, Cioffi MDB (2019) Deciphering the origin and evolution of the X1X2Y system in two closely-related Oplegnathus species (Oplegnathidae and Centrarchiformes). Int J Mol Sci 20:3571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Yang F, Chen R, Lou B, Zhan W, Hayashida T, Takeuchi Y (2018) Production of neo-males from gynogenetic yellow drum through 17α-methyltestosterone immersion and subsequent application for the establishment of all-female populations. Aquaculture 489:154–161

    Article  CAS  Google Scholar 

  • Xu G, Huang T, Gu W, Liu E, Wang B (2021) Effects of letrozole and 17α-methyltestosterone on gonadal development in all-female triploid rainbow trout (Oncorhynchus mykiss). Aquac Res 00:1–10

    Google Scholar 

  • Xue R, An H, Liu QH, Xiao ZZ, Wang YF, Li J (2016) Karyotype and Ag-NORs in male and female of Oplegnathus Punctatus. Ocean Limnol 47:626–632

    Google Scholar 

  • Yamamoto TO (1969) Sex differentiation. In Fish Physiology 3:117–175

    Article  CAS  Google Scholar 

  • Yang F, Ye H, Takeuchi Y, Liu F, Xu D (2021) Characterization of the sex differentiation and gonadal development in small yellow croaker (Larimichthys polyactis) and its hybrid (L. polyactis ♀ × L. crocea ♂). Fish Physiol Biochem 47:1467–1476

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Chen Z, Ma T, Li M, Wu Y, Wang Q, Chen S (2021) Histological observation and preliminary analysis of gonad development in spotted knifejaw (Oplegnathus punctatus). J Shanghai Ocean Univ 30:675–683

    Google Scholar 

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Funding

This work was supported by grants from the Zhejiang Provincial Natural Science Foundation of China (No. LQ20C190008) and National Key R&D Program of China (2019YFD0901204).

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Authors and Affiliations

  1. School of Fisheries, Zhejiang Ocean University, Zhoushan, China

    Mingtao Liu & Huan Li

  2. Key Lab of Mariculture and Enhancement of Zhejiang Province, Zhejiang Marine Fisheries Research Institute, Zhoushan, China

    Mingtao Liu, Qihui Zhu, Huan Li, Ruiyi Chen, Weihua Hu, Simiao Liu & Dongdong Xu

  3. Ocean and Fisheries Research Institute, Zhejiang Ocean University, Zhoushan, China

    Qihui Zhu, Ruiyi Chen, Weihua Hu & Dongdong Xu

  4. School of Marine Sciences, Ningbo University, Ningbo, China

    Simiao Liu

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  1. Mingtao Liu
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Contributions

Q. Z. and D. X. designed the experiments. M. L., Q. Z., H. L., R. C., W. H., and S. L. performed the research, while M. L., Q. Z., and D. X. wrote the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Dongdong Xu.

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Mingtao Liu and Qihui Zhu have contributed equally to this work

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Liu, M., Zhu, Q., Li, H. et al. Characterization of Early Gonadal Differentiation and Induction of Sex Reversal in the Rock Bream Oplegnathus fasciatus. Mar Biotechnol 25, 403–414 (2023). https://doi.org/10.1007/s10126-023-10213-8

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