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Comparative transcriptome analysis of male and female gonads reveals sex-biased genes in spotted scat (Scatophagus argus)

  • Fei-Xiang He
  • Dong-Neng Jiang
  • Yuan-Qing Huang
  • Umar Farouk Mustapha
  • Wei Yang
  • Xue-Fan Cui
  • Chang-Xu Tian
  • Hua-Pu Chen
  • Hong-Juan Shi
  • Si-Ping Deng
  • Guang-Li Li
  • Chun-Hua ZhuEmail author
Article

Abstract

Scatophagus argus is a new emerging aquaculture fish in East and Southeast Asia. To date, research on reproductive development and regulation in S. argus is lacking. Additionally, genetic and genomic information about reproduction, such as gonadal transcriptome data, is also lacking. Herein, we report the first gonadal transcriptomes of S. argus and identify genes potentially involved in reproduction and gonadal development. A total of 136,561 unigenes were obtained by sequencing of testes (n = 3) and ovaries (n = 3) at stage III. Genes upregulated in males and females known to be involved in gonadal development and gametogenesis were identified, including male-biased dmrt1, amh, gsdf, wt1a, sox9b, and nanos2, and female-biased foxl2, gdf9, bmp15, sox3, zar1, and figla. Serum estradiol-17β and 11-ketotestosterone levels were biased in female and male fish, respectively. Sexual dimorphism of serum steroid hormone levels were interpreted after expression analysis of 20 steroidogenesis-related genes, including cyp19a1a and cyp11b2. This gonadal transcript dataset will help investigate functional genes related to reproduction in S. argus.

Keywords

Scatophagus argus Transcriptome Gonad Sex determination and differentiation Sex steroid hormone 

Notes

Authors’ contributions

FXH and DNJ carried out the experiments, performed the statistical analyses, and drafted the manuscript. YQH, UFM, WY, XFC, and CXT performed the experiments. HPC, HJS, SPD, and GLL participated in protocol development and data analysis. CHZ and DNJ designed and supervised the experiments, analyzed the data, and critically edited the manuscript. All authors read and approved the final manuscript.

Funding information

This work was funded by Grants from Key Project of “Blue Granary Science and Technology Innovation” of the Ministry of Science and Technology (2018YFD0901203), grants from NSFC of China (31702326 and 41706174), Natural Science Foundation of Guangdong Province (2016A030313743, 2017A030313101, and 2018B030311050), grant from the Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams (2019KJ149), grant from the Department of Education of Guangdong Province (2018KTSCX090 and 2018KQNCX106), Zhanjiang Science and Technology Bureau (2016A03017), Guangdong Ocean University Natural Science Research Program (2015 and 2016), Project of Provincial Key Platform and Major Scientific Research of Colleges and Universities in Guangdong (2015KTSCX058), Sail Projects of Guangdong (2014.1), Marine Fishery Science and Technology Extension Projects of Guangdong (A201408A06 and A201608B01), and Program for Scientific Research Start-up Funds of Guangdong Ocean University.

Compliance with ethical standards

Animal ethics

All experimental protocols involved in this study were approved by the Regulations for the Administration of Affairs Concerning Experimental Animals for the Science and Technology Bureau of China. Experiments involving S. argus were approved by the Animal Research and Ethics Committee of Guangdong Ocean University.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10695_2019_693_MOESM1_ESM.docx (752 kb)
ESM 1 (DOCX 751 kb)
10695_2019_693_MOESM2_ESM.xlsx (2.9 mb)
ESM 2 (XLSX 2997 kb)

References

  1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106.  https://doi.org/10.1186/gb-2010-11-10-r106 Google Scholar
  2. Bellaiche J, Lareyre JJ, Cauty C, Yano A, Allemand I, Le Gac F (2014) Spermatogonial stem cell quest: nanos2, marker of a subpopulation of undifferentiated A spermatogonia in trout testis. Biol Reprod 90(4):79–71.  https://doi.org/10.1095/biolreprod.113.116392 Google Scholar
  3. Boulanger L, Pannetier M, Gall L, Allais-Bonnet A, Elzaiat M, Le Bourhis D, Daniel N, Richard C, Cotinot C, Ghyselinck NB, Pailhoux E (2014) FOXL2 is a female sex-determining gene in the goat. Curr Biol 24(4):404–408.  https://doi.org/10.1016/j.cub.2013.12.039 Google Scholar
  4. Cai ZP, Wang Y, Hu JW, Zhang JB, Lin YG (2010) Reproductive biology of Scatophagus argus and artificial induction of spawning. J Trop Oceanogr 29(5):180–185Google Scholar
  5. Cavaco JEB, Bogerd J, Goos H, Schulz RW (2001) Testosterone inhibits 11-ketotestosterone-induced spermatogenesis in African catfish (Clarias gariepinus). Biol Reprod 65(6):1807–1812Google Scholar
  6. Chandler JC, Fitzgibbon QP, Smith G, Elizur A, Ventura T (2017) Y-linked iDmrt1 paralogue (iDMY) in the Eastern spiny lobster, Sagmariasus verreauxi: the first invertebrate sex-linked Dmrt. Dev Biol 430(2):337–345.  https://doi.org/10.1016/j.ydbio.2017.08.031 Google Scholar
  7. Chen J, He M, Yan B, Zhang J, Jin S, Liu L (2015) Molecular characterization of dax1 and SF-1 and their expression analysis during sex reversal in spotted scat, Scatophagus argus. J World Aquacult Soc 46(1):1–19.  https://doi.org/10.1111/jwas.12165 Google Scholar
  8. Chen L, Jiang X, Feng H, Shi H, Sun L, Tao W, Xie Q, Wang D (2016) Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption. J Endocrinol 228(3):205–218.  https://doi.org/10.1530/JOE-15-0432 Google Scholar
  9. Chen W, Liu L, Ge W (2017) Expression analysis of growth differentiation factor 9 (Gdf9/gdf9), anti-Müllerian hormone (Amh/amh) and aromatase (Cyp19a1a/cyp19a1a) during gonadal differentiation of the zebrafish, Danio rerio. Biol Reprod 96(2):401–413.  https://doi.org/10.1095/biolreprod.116.144964 Google Scholar
  10. Cui D, Liu ZW, Liu NX, Zhang YY, Zhang JB (2013) Histological study on the gonadal development of Scatophagus argus. J Fish China 37(5):696–704Google Scholar
  11. Cui XF, Zhao Y, Chen HP, Deng SP, Jiang DN, Wu TL, Zhu CH, Li GL (2017) Cloning, expression and functional characterization on vitellogenesis of estrogen receptors in Scatophagus argus. Gen Comp Endocrinol 246:37–45.  https://doi.org/10.1016/j.ygcen.2017.03.002 Google Scholar
  12. Deng SP, Wu B, Zhu CH, Li GL (2014) Molecular cloning and dimorphic expression of growth hormone (gh) in female and male spotted scat Scatophagus argus. Fish Sci 80(4):715–723.  https://doi.org/10.1007/s12562-014-0763-5 Google Scholar
  13. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 208(3–4):191–364.  https://doi.org/10.1016/S0044-8486(02)00057-1 Google Scholar
  14. Dranow DB, Hu K, Bird AM, Lawry ST, Adams MT, Sanchez A, Amatruda JF, Draper BW (2016) Bmp15 is an oocyte-produced signal required for maintenance of the adult female sexual phenotype in zebrafish. PLoS Genet 12(9):e1006323.  https://doi.org/10.1371/journal.pgen.1006323 Google Scholar
  15. Du X, Wang B, Liu X, Liu X, He Y, Zhang Q, Wang X (2017) Comparative transcriptome analysis of ovary and testis reveals potential sex-related genes and pathways in spotted knifejaw Oplegnathus punctatus. Gene. 637:203–210.  https://doi.org/10.1016/j.gene.2017.09.055 Google Scholar
  16. Fakriadis I, Lisi F, Sigelaki I, Papadaki M, Mylonas CC (2018) Spawning kinetics and egg/larval quality of greater amberjack (Seriola dumerili) in response to multiple GnRHa injections or implants. Gen Comp Endocrinol 279:78–87.  https://doi.org/10.1016/j.ygcen.2018.12.007 Google Scholar
  17. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, Behringer RR, Lécureuil C, Guillou F, Huff V (2006) The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc Natl Acad Sci 103(32):11987–11992.  https://doi.org/10.1073/pnas.0600994103 Google Scholar
  18. Garber M, Grabherr MG, Guttman M, Trapnell C (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 8(6):469–477.  https://doi.org/10.1038/nmeth.1613 Google Scholar
  19. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644–652.  https://doi.org/10.1038/nbt.1883 Google Scholar
  20. 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(3):352–366.  https://doi.org/10.1016/j.ygcen.2009.03.002 Google Scholar
  21. Gupta S (2016) An overview on morphology, biology, and culture of spotted scat Scatophagus argus (Linnaeus 1766). Rev Fish Sci Aquac 24(2):203–212.  https://doi.org/10.1080/23308249.2015.1119800 Google Scholar
  22. Hao L, Wei X, Zhu J, Shi J, Liu J, Gu H, Tsuge T, Qu LJ (2017) SNAIL1 is essential for female gametogenesis in Arabidopsis thaliana. J Integr Plant Biol 59(9):629–641.  https://doi.org/10.1111/jipb.12572 Google Scholar
  23. Herpin A, Schartl M (2011) Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 278(7):1010–1019.  https://doi.org/10.1111/j.1742-4658.2011.08030.x Google Scholar
  24. Hirst CE, Major AT, Ayers KL, Brown RJ, Mariette M, Sackton TB, Smith CA (2017) Sex reversal and comparative data undermine the W chromosome and support Z-linked DMRT1 as the regulator of gonadal sex differentiation in birds. Endocrinology. 158(9):2970–2987.  https://doi.org/10.1210/en.2017-00316 Google Scholar
  25. Hong Q, Li C, Ying R, Lin H, Li J, Zhao Y, Cheng H, Zhou R (2019) Loss-of-function of sox3 causes follicle development retardation and reduces fecundity in zebrafish. Protein Cell 10:1–18.  https://doi.org/10.1007/s13238-018-0603-y Google Scholar
  26. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nagahama Y (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78(2):333–341Google Scholar
  27. Imai T, Saino K, Matsuda M (2015) Mutation of gonadal soma-derived factor induces medaka XY gonads to undergo ovarian development. Biochem Biophys Res Commun 467(1):109–114.  https://doi.org/10.1016/j.bbrc.2015.09.112 Google Scholar
  28. Jeng SR, Wu GC, Yueh WS, Kuo SF, Dufour S, Chang CF (2018) Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel. Gen Comp Endocrinol 257:74–85.  https://doi.org/10.1016/j.ygcen.2017.07.031 Google Scholar
  29. Jiang DN, Yang HH, Li MH, Shi HJ, Zhang XB, Wang DS (2016) gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia. Mol Reprod Dev 83(6):497–508.  https://doi.org/10.1002/mrd.22642 Google Scholar
  30. Jiang DN, Li JT, Tao YX, Chen HP, Deng SP, Zhu CH, Li GL (2017a) Effects of melanocortin-4 receptor agonists and antagonists on expression of genes related to reproduction in spotted scat, Scatophagus argus. J Comp Physiol B 187(4):603–612.  https://doi.org/10.1007/s00360-017-1062-0 Google Scholar
  31. Jiang DN, Chen JL, Fan Z, Tan DJ, Zhao JE, Shi HJ, Liu ZL, Tao WJ, Li MH, Wang DS (2017b) CRISPR/Cas9-induced disruption of wt1a and wt1b reveals their different roles in kidney and gonad development in Nile tilapia. Dev Biol 428(1):63–73.  https://doi.org/10.1016/j.ydbio.2017.05.017 Google Scholar
  32. Jiang DN, Mustapha UF, Shi HJ, Huang YQ, Si-Tu JX, Wang M, Deng SP, Chen HP, Tian CX, Zhun CH, Li GL (2019) Expression and transcriptional regulation of gsdf in spotted scat (Scatophagus argus). Comp Biochem Physiol B: Biochem Mol Biol 233:35–45Google Scholar
  33. Joshi S, Davies H, Sims LP, Levy SE, Dean J (2007) Ovarian gene expression in the absence of FIGLA, an oocyte-specific transcription factor. BMC Dev Biol 7(1):67.  https://doi.org/10.1186/1471-213X-7-67 Google Scholar
  34. Klüver N, Kondo M, Herpin A, Mitani H, Schartl M (2005) Divergent expression patterns of Sox9 duplicates in teleosts indicate a lineage specific subfunctionalization. Dev Genes Evol 215(6):297–305.  https://doi.org/10.1007/s00427-005-0477-x Google Scholar
  35. Klüver N, Pfennig F, Pala I, Storch K, Schlieder M, Froschauer A, Gutzeit HO, Schartl M (2007) Differential expression of anti-Müllerian hormone (amh) and anti-Müllerian hormone receptor type II (amhrII) in the teleost medaka. Dev Dyn 236(1):271–281.  https://doi.org/10.1002/dvdy.20997 Google Scholar
  36. Koya Y, Soyano K, Yamamoto K, Obana H, Matsubara T (2002) Testicular development and serum profiles of steroid hormone levels in captive male Pacific herring Clupea pallasii during their first maturational cycle. Fish Sci 68(5):1099–1105Google Scholar
  37. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1):323.  https://doi.org/10.1186/1471-2105-12-323 Google Scholar
  38. Li S, Liu Z, Hu P, Liang XM, Liu HF, Su ML, Zhang JB (2014a) SNP discovery using high-throughput 454 pyrosequencing and validation in the spotted scat, Scatophagus argus. Conserv Genet Resour 6(4):817–820.  https://doi.org/10.1007/s12686-014-0255-z Google Scholar
  39. Li MH, Yang HH, Zhao JE, Fang LL, Shi HJ, Li MR, Sun YL, Zhang XB, Jiang DN, Zhou LY, Wang DS (2014b) Efficient and heritable gene targeting in tilapia by CRISPR/Cas9. Genetics. 197(2):591–599.  https://doi.org/10.1534/genetics.114.163667 Google Scholar
  40. Li GL, Zhang MZ, Deng SP, Chen HP, Zhu CH (2015) Effects of temperature and fish oil supplementation on ovarian development and foxl2 mRNA expression in spotted scat Scatophagus argus. J Fish Biol 86(1):248–260.  https://doi.org/10.1111/jfb.12578 Google Scholar
  41. Lin Q, Mei J, Li ZH, Zhang X, Zhou L, Gui JF (2017) Distinct and cooperative roles of amh and dmrt1 in self-renewal and differentiation of male germ cells in zebrafish. Genetics. 207(3):1007–1022.  https://doi.org/10.1534/genetics.117.300274 Google Scholar
  42. Liu H, Mu X, Gui L, Su M, Li H, Zhang G, Liu Z, Zhang JB (2015) Characterization and gonadal expression of FOXL2 relative to Cyp19a genes in spotted scat Scatophagus argus. Gene. 561(1):6–14.  https://doi.org/10.1016/j.gene.2014.12.060 Google Scholar
  43. Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T, Nagahama Y, Matsuda M (2012) Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosom Res 20(1):163–176.  https://doi.org/10.1007/s10577-011-9264-x Google Scholar
  44. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 417(6888):559–563.  https://doi.org/10.1038/nature751 Google Scholar
  45. Mei J, Gui JF (2015) Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sci China Life Sci 58(2):124–136.  https://doi.org/10.1007/s11427-014-4797-9 Google Scholar
  46. Miao L, Yuan Y, Cheng F, Fang J, Zhou F, Ma W, Jiang Y, Huang X, Wang Y, Shan L, Chen D (2017) Translation repression by maternal RNA binding protein Zar1 is essential for early oogenesis in zebrafish. Development. 144(1):128–138.  https://doi.org/10.1242/dev.144642 Google Scholar
  47. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5(7):621–628.  https://doi.org/10.1038/nmeth.1226 Google Scholar
  48. Mu X, Su M, Gui L, Liang X, Zhang P, Hu P, Liu Z, Zhang JB (2015) Comparative renal gene expression in response to abrupt hypoosmotic shock in spotted scat (Scatophagus argus). Gen Comp Endocrinol 215:25–35.  https://doi.org/10.1016/j.ygcen.2014.09.017 Google Scholar
  49. Mustapha UF, Jiang DN, Liang ZH, Gu HT, Yang W, Chen HP, Deng SP, Wu TL, Tian CX, Zhu CH, Li GL (2018) Male-specific Dmrt1 is a candidate sex determination gene in spotted scat (Scatophagus argus). Aquaculture. 495:351–358.  https://doi.org/10.1016/j.aquaculture.2018.06.009 Google Scholar
  50. Nakamoto M, Shibata Y, Ohno K, Usami T, Kamei Y, Taniguchi Y, Todo T, Sakamoto T, Young G, Swanson P, Naruse K (2018) Ovarian aromatase loss-of-function mutant medaka undergo ovary degeneration and partial female-to-male sex reversal after puberty. Mol Cell Endocrinol 460:104–122.  https://doi.org/10.1016/j.mce.2017.07.013 Google Scholar
  51. Nakamura S, Watakabe I, Nishimura T, Picard JY, Toyoda A, Taniguchi Y, di Clemente N, Tanaka M (2012a) Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development. 139(13):2283–2287.  https://doi.org/10.1242/dev.076307 Google Scholar
  52. Nakamura S, Watakabe I, Nishimura T, Toyoda A, Taniguchi Y, Tanaka M (2012b) Analysis of medaka sox9 orthologue reveals a conserved role in germ cell maintenance. PLoS One 7(1):e29982.  https://doi.org/10.1371/journal.pone.0029982 Google Scholar
  53. Naor Z (2009) Signaling by G-protein-coupled receptor (GPCR): studies on the GnRH receptor. Front Neuroendocrinol 30(1):10–29.  https://doi.org/10.1016/j.yfrne.2008.07.001 Google Scholar
  54. Paul-Prasanth B, Bhandari RK, Kobayashi T, Horiguchi R, Kobayashi Y, Nakamoto M, Shibata Y, Sakai F, Nakamura M, Nagahama Y (2013) Estrogen oversees the maintenance of the female genetic program in terminally differentiated gonochorists. Sci Rep 3:2862.  https://doi.org/10.1038/srep02862 Google Scholar
  55. Perner B, Englert C, Bollig F (2007) The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol 309(1):87–96.  https://doi.org/10.1016/j.ydbio.2007.06.022 Google Scholar
  56. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics. 19(5):651–652.  https://doi.org/10.1093/bioinformatics/btg034 Google Scholar
  57. Qin M, Zhang Z, Song W, Wong QWL, Chen W, Shirgaonkar N, Ge W (2018) Roles of Figla/figla in juvenile ovary development and follicle formation during zebrafish gonadogenesis. Endocrinology. 159(11):3699–3722.  https://doi.org/10.1210/en.2018-00648 Google Scholar
  58. Qiu Y, Sun S, Charkraborty T, Wu L, Sun L, Wei J, Nagahama Y, Wang D, Zhou L (2015) Figla favors ovarian differentiation by antagonizing spermatogenesis in a teleosts, Nile tilapia (Oreochromis niloticus). PLoS One 10(4):e0123900.  https://doi.org/10.1371/journal.pone.0123900 Google Scholar
  59. Raghuveer K, Senthilkumaran B, Sudhakumari CC, Sridevi P, Rajakumar A, Singh R, Murugananthkumar R, Majumdar KC (2011) Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sex Dev 5(4):213–223.  https://doi.org/10.1159/000328823 Google Scholar
  60. Rajpert-De Meyts E, Jørgensen N, Græm N, Müller J, Cate RL, Skakkebæk NE (1999) Expression of anti-Mullerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 84(10):3836–3844.  https://doi.org/10.1210/jcem.84.10.6047 Google Scholar
  61. Roy A, Basak R, Rai U (2017) De novo sequencing and comparative analysis of testicular transcriptome from different reproductive phases in freshwater spotted snakehead Channa punctatus. PLoS One 12(3):e0173178Google Scholar
  62. Sada A, Suzuki A, Suzuki H, Saga Y (2009) The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science. 325(5946):1394–1398.  https://doi.org/10.1126/science.1172645 Google Scholar
  63. Sawatari E, Shikina S, Takeuchi T, Yoshizaki G (2007) A novel transforming growth factor-β superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev Biol 301(1):266–275.  https://doi.org/10.1016/j.ydbio.2006.10.001 Google Scholar
  64. Shi HJ, Gao T, Liu ZL, Sun LN, Jiang XL, Chen L, Wang DS (2017) Blockage of androgen and administration of estrogen induce transdifferentiation of testis into ovary. J Endocrinol 233(1):65–80.  https://doi.org/10.1530/JOE-16-0551 Google Scholar
  65. Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y (2010) Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10(6):283–289.  https://doi.org/10.1016/j.gep.2010.06.005 Google Scholar
  66. Silva BDM, Castro EA, Souza CJH, Paiva SR, Sartori R, Franco MM, Azevedo HC, Silva TASN, Vieira AMC, Neves JP, Melo EDO (2011) A new polymorphism in the growth and differentiation factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep. Anim Genet 42(1):89–92.  https://doi.org/10.1111/j.1365-2052.2010.02078.x Google Scholar
  67. Sivan G, Radhakrishnan CK (2011) Food, feeding habits and biochemical composition of Scatophagus argus. Turk J Fish Aquat Sci 11(4):603–608.  https://doi.org/10.4194/1303-2712-v11-4-14 Google Scholar
  68. Stocco DM (2000) The role of the StAR protein in steroidogenesis: challenges for the future. J Endocrinol 164(3):247–253.  https://doi.org/10.1677/joe.0.1640247 Google Scholar
  69. Su L, Zhou F, Ding Z, Gao Z, Wen J, Wei W, Wang Q, Wang W, Liu H (2015) Transcriptional variants of Dmrt1 and expression of four Dmrt genes in the blunt snout bream, Megalobrama amblycephala. Gene. 573(2):205–215.  https://doi.org/10.1016/j.gene.2015.07.044 Google Scholar
  70. Su M, Mu X, Gui L, Zhang P, Zhou J, Ma J, Zhang J (2016) Dopamine regulates renal osmoregulation during hyposaline stress via DRD1 in the spotted scat (Scatophagus argus). Sci Rep 6:37535.  https://doi.org/10.1038/srep37535 Google Scholar
  71. Sun F, Liu S, Gao X, Jiang Y, Perera D, Wang X, Li C, Sun L, Zhang J, Kaltenboeck L, Dunham R (2013) Male-biased genes in catfish as revealed by RNA-seq analysis of the testis transcriptome. PLoS One 8(7):e68452.  https://doi.org/10.1371/journal.pone.0068452 Google Scholar
  72. Sun LN, Jiang XL, Xie QP, Yuan J, Huang BF, Tao WJ, Zhou LY, Nagahama Y, Wang DS (2014) Transdifferentiation of differentiated ovary into functional testis by long-term treatment of aromatase inhibitor in Nile tilapia. Endocrinology. 155(4):1476–1488.  https://doi.org/10.1210/en.2013-1959 Google Scholar
  73. Sutton E, Hughes J, White S, Sekido R, Tan J, Arboleda V, Rogers N, Knower K, Rowley L, Eyre H, Rizzoti K (2011) Identification of SOX3 as an XX male sex reversal gene in mice and humans. J Clin Invest 121(1):328–341.  https://doi.org/10.1172/JCI42580 Google Scholar
  74. Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28(1–4):53–59.  https://doi.org/10.1023/B:FISH.0000030476.73360.07 Google Scholar
  75. Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin T, Kohara Y, Kuroki Y, Toyoda A, Fujiyama A, Hamaguchi S (2014) Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun 5:4157.  https://doi.org/10.1038/ncomms5157 Google Scholar
  76. Tao W, Yuan J, Zhou LY, Sun LN, Sun YL, Yang SJ, Li MH, Zeng S, Huang BF, Wang DS (2013) Characterization of gonadal transcriptomes from Nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS One 8(5):e63604.  https://doi.org/10.1371/journal.pone.0063604 Google Scholar
  77. Tao WJ, Chen JL, Tan DJ, Yang J, Sun LN, Wei J, Conte MA, Kocher TD, Wang DS (2018) Transcriptome display during tilapia sex determination and differentiation as revealed by RNA-seq analysis. BMC Genomics 19(1):363.  https://doi.org/10.1186/s12864-018-4756-0 Google Scholar
  78. Wang L, Feng Z, Wang X, Wang X, Zhang X (2009) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138.  https://doi.org/10.1093/bioinformatics/btp612 Google Scholar
  79. Wang W, Zhu H, Dong Y, Tian Z, Dong T, Hu H, Niu C (2017) Dimorphic expression of sex-related genes in different gonadal development stages of sterlet, Acipenser ruthenus, a primitive fish species. Fish Physiol Biochem 43(6):1557–1569Google Scholar
  80. Wei L, Yang C, Tao WJ, Wang DS (2016) Genome-wide identification and transcriptome-based expression profiling of the sox gene family in the Nile tilapia (Oreochromis niloticus). Int J Mol Sci 17(3):270.  https://doi.org/10.3390/ijms17030270 Google Scholar
  81. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL (2003) Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 23(22):8084–8091.  https://doi.org/10.1128/MCB.23.22.8084-8091.2003 Google Scholar
  82. Wu X, Wang P, Brown CA, Zilinski CA, Matzuk MM (2003) Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol Reprod 69(3):861–867.  https://doi.org/10.1095/biolreprod.103.016022 Google Scholar
  83. Wu J, Xiong S, Jing J, Chen X, Wang W, Gui JF, Mei J (2015) Comparative transcriptome analysis of differentially expressed genes and signaling pathways between XY and YY testis in yellow catfish. PLoS One 10(8):e0134626.  https://doi.org/10.1371/journal.pone.0134626 Google Scholar
  84. Yan H, Shen X, Cui X, Wu Y, Wang L, Zhang L, Liu Q, Jiang Y (2018) Identification of genes involved in gonadal sex differentiation and the dimorphic expression pattern in Takifugu rubripes gonad at the early stage of sex differentiation. Fish Physiol Biochem 44(5):1275–1290.  https://doi.org/10.1007/s10695-018-0519-8 Google Scholar
  85. Yang YJ, Wang Y, Li Z, Zhou L, Gui JF (2017) Sequential, divergent, and cooperative requirements of Foxl2a and Foxl2b in ovary development and maintenance of zebrafish. Genetics. 205(4):1551–1572.  https://doi.org/10.1534/genetics.116.199133 Google Scholar
  86. Yang W, Chen HP, Cui XF, Zhang KW, Jiang DN, Deng SP, Zhu CH, Li GL (2018) Sequencing, de novo assembly and characterization of the spotted scat Scatophagus argus (Linnaeus 1766) transcriptome for discovery of reproduction related genes and SSRs. J Oceanol Limnol 36(4):1329–1134.  https://doi.org/10.1007/s00343-018-7090-0 Google Scholar
  87. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(2):W293–W297.  https://doi.org/10.1093/nar/gkl031 Google Scholar
  88. Yu X, Wu L, Xie L, Yang S, Charkraborty T, Shi HJ, Wang DS, Zhou LY (2014) Characterization of two paralogous StAR genes in a teleost, Nile tilapia (Oreochromis niloticus). Mol Cell Endocrinol 392(1–2):152–162.  https://doi.org/10.1016/j.mce.2014.05.013 Google Scholar
  89. Zhang MZ, Li GL, Zhu CH, Deng SP (2013) Effects of fish oil on ovarian development in spotted scat (Scatophagus argus). Anim Reprod Sci 141(1–2):90–97.  https://doi.org/10.1016/j.anireprosci.2013.06.020 Google Scholar
  90. Zhang X, Guan G, Li M, Zhu F, Liu Q, Naruse K, Herpin A, Nagahama Y, Li J, Hong Y (2016) Autosomal gsdf acts as a male sex initiator in the fish medaka. Sci Rep 6:19738.  https://doi.org/10.1038/srep19738 Google Scholar
  91. Zhang XB, Li MR, Ma H, Liu XY, Shi HJ, Li MH, Wang DS (2017) Mutation of foxl2 or cyp19a1a results in female to male sex reversal in XX Nile tilapia. Endocrinology. 158(8):2634–2647.  https://doi.org/10.1210/en.2017-00127 Google Scholar
  92. Zhang G, Wang W, Su M, Zhang J (2018) Effects of recombinant gonadotropin hormones on the gonadal maturation in the spotted scat, Scatophagus argus. Aquaculture. 483:263–272.  https://doi.org/10.1016/j.aquaculture.2017.10.017 Google Scholar
  93. Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165(3):438–455.  https://doi.org/10.1016/j.ygcen.2009.04.017 Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Fei-Xiang He
    • 1
  • Dong-Neng Jiang
    • 1
  • Yuan-Qing Huang
    • 1
  • Umar Farouk Mustapha
    • 1
  • Wei Yang
    • 1
  • Xue-Fan Cui
    • 1
  • Chang-Xu Tian
    • 1
  • Hua-Pu Chen
    • 1
  • Hong-Juan Shi
    • 1
  • Si-Ping Deng
    • 1
  • Guang-Li Li
    • 1
  • Chun-Hua Zhu
    • 1
    Email author
  1. 1.Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Key Laboratory of Aquaculture in South China Sea for Aquatic Economic Animal of Guangdong Higher Education Institutes, Fisheries CollegeGuangdong Ocean UniversityZhanjiangChina

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