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Expression profiles of amh and foxl2 in Schizothorax kozlovi, and their response to temperature during the early developmental stage

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Abstract

To elucidate the role of amh and foxl2 in sex differentiation of the teleost fish Schizothorax kozlovi, the full-length cDNAs were cloned from the mature testis and ovary by rapid amplification of cDNA ends (RACE), and their relative mRNA expression levels were determined by quantitative real-time polymerase chain reaction among tissues and temperature groups. The complete amh and foxl2 cDNAs of S. kozlovi were 2060 bp and 1750 bp, which encoded 568 and 306 amino acids, respectively. The amh were expressed only in gonads, while foxl2 was expressed in the gills, brain and gonads, both exhibiting relatively high tissue specificity. The amh exhibited sex-specific expression pattern in the gonads. No sex differences in the foxl2 expression were observed in the brain and gonads, but significant sex differences were found in the gills. No significant differences were found in the foxl2 expression, from the larval to the juvenile stage, and also between different temperature groups. However, significant differences were found in the expression levels of amh from the larval (12–63 days posthatching (dph)) to the juvenile stage (190 dph), and also among the \(18{^{\circ }}\hbox {C}\) and \(10{^{\circ }}\hbox {C}\) groups at 31 dph. This result suggested that amh plays an important role in male sex differentiation of S. kozlovi during the early developmental stage, but no similar effect was observed in foxl2.

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References

  • Ashida H., Ueyama N., Kinoshita M. and Kobayashi T. 2013 Molecular identification and expression of FOXL2 and DMRT1 genes from willow minnow Gnathopogon caerulescens. Reprod. Biol. 13, 317–324.

    Article  PubMed  Google Scholar 

  • Baroiller J. F., D’Cotta H. and Saillant E. 2009 Environmental effects on fish sex determination and differentiation. Sex. Dev. 3, 118–135.

    Article  CAS  PubMed  Google Scholar 

  • Baron D., Houlgatte R., Fostier A. and Guiguen Y. 2005 Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol. Reprod. 73, 959–966.

    Article  CAS  PubMed  Google Scholar 

  • Chen Y. X. 2013 The genetic characterization and population genetic diversity of Schizothorax kozlovi (Nikolsky). Dissertation of Sichuan Agricultural University, Yaan.

    Google Scholar 

  • Conover D. O. and Kynard B. E. 1981 Environmental sex determination: interaction of temperature and genotypes in a fish. Science 213, 577–579.

    Article  CAS  PubMed  Google Scholar 

  • Díaz N. and Piferrer F. 2015 Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination. BMC Genomics 16, 679.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong X. L., Chen S. L., Ji X. S. and Shao C. W. 2011 Molecular cloning, characterization and expression analysis of Sox9a and Foxl2 genes in half-smooth tongue sole (Cynoglossus semilaevis). Acta Oceanol. Sin. 30, 68–77.

    Article  CAS  Google Scholar 

  • Fernandino J. I., Hattori R. S., Kimura H., Strüssmann C. A. and Somoza G. A. 2008 Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature-dependent sex determination. Dev. Dyn. 237, 3192–3199.

    Article  CAS  PubMed  Google Scholar 

  • Filby A. L., Thorpe K. L., Maack G. and Tyler C. R. 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 

  • He Y. F., Wu X. B., Zhu Y. J. and Yang D. G. 2016a Cloning of gonadal aromatase gene Cyp19\(a\) in an endemic fish (Schizothorax kozlovi) of the upper Yangtze River, and temperature effects on its expression. Genes Genom. 38, 841–848.

    Article  CAS  Google Scholar 

  • He Y. F., Zhu Y. J., Guo W., Yang D. G. and Wu X. B. 2016b Tissue distribution of brain aromatase gene Cyp19\(b\) in Schizothorax kozlovi and temperature effects on its expression. Chin. J. Zool. 51, 281–290.

    Google Scholar 

  • Huelsenbeck J. P. and Ronquist F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, S754–S755.

    Article  Google Scholar 

  • Ijiri S., Kaneko H., Kobayashi T., Wang D. S., Sakai F., Paul-Prasanth B. et al. 2008 Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 78, 333–341.

    Article  CAS  PubMed  Google Scholar 

  • Kitano T., Yoshinaga N., Shiraishi E., Koyanagi T. and Abe S. 2007 Tamoxifen induces masculinization of genetic females and regulates P450 aromatase and Müllerian inhibiting substance mRNA expression in Japanese flounder (Paralichthys olivaceus). Mol. Reprod. Dev. 74, 1171–1177.

    Article  CAS  PubMed  Google Scholar 

  • Klüver N., Pfennig F., Pala I., Storch K., Schlieder M., Froschauer A. et al. 2007 Differential expression of anti-Müllerian hormone (amh) and anti-Müllerian hormone receptor type II (amhrII) in the teleost medaka. Dev. Dyn. 236, 271–281.

    Article  PubMed  Google Scholar 

  • Kobayashi Y., Horiguchi R., Nozu R. and Nakamura M. 2010 Expression and localization of forkhead transcriptional factor 2 (Foxl2) in the gonads of protogynous wrasse, Halichoeres trimaculatus. Biol. Sex. Differ. 1, 3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C. G., Wang H., Chen H. J., Zhao Y., Fu P. S. and Ji X. S. 2014 Differential expression analysis of genes involved in high-temperature induced sex differentiation in Nile tilapia. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 177–178, 36–45.

    Article  Google Scholar 

  • Liu X. L., Liu J. G. and Zhang Z. F. 2013 Structure and expression regulation of gene foxl2. Period. Ocean. U. China 43, 38–43.

    Google Scholar 

  • Mei J. and Gui J. F. 2014 Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sci. China Life Sci. 44, 1198–1212.

    Google Scholar 

  • Morinaga C., Saito D., Nakamura S., Sasaki T., Asakawa S., Shimizu N. et al. 2007 The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc. Natl. Acad. Sci. USA 104, 9691–9696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura S., Kobayashi D., Aoki Y., Yokoi H., Ebe Y., Wittbrodt J. and Tanaka M. 2006 Identification and lineage tracing of two populations of somatic gonadal precursors in medaka embryos. Dev. Biol. 295, 678–688.

    Article  CAS  PubMed  Google Scholar 

  • Oshima Y., Uno Y., Matsuda Y., Kobayashi T. and Nakamura M. 2008 Molecular cloning and gene expression of Foxl2 in the frog Rana rugose. Gen. Comp. Endocrinol. 159, 170–177.

    Article  CAS  PubMed  Google Scholar 

  • Ospina-Álvarez N. and Piferrer F. 2008 Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 3, e2837.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pala I., Klüver N., Thorsteinsdóttir S., Schartl M. and Coelhom M. M. 2008 Expression pattern of anti-Müllerian hormone (amh) in the hybrid fish complex of Squalius alburnoides. Gene 410, 249–258.

    Article  CAS  PubMed  Google Scholar 

  • Pfennig F., Standke A. and Gutzeit H. O. 2015 The role of Amh signaling in teleost fish – Multiple functions not restricted to the gonads. Gen. Comp. Endocrinol. 223, 87–107.

    Article  CAS  PubMed  Google Scholar 

  • Poonlaphdecha S., Pepey E., Canonne M., de Verdal H., Baroiller J. F. and D’Cotta H. 2013 Temperature induced-masculinisation in the Nile tilapia causes rapid upregulation of both dmrt1 and amh expressions. Gen. Comp. Endocrinol. 193, 234–242.

    Article  CAS  PubMed  Google Scholar 

  • Posada D. and Crandall K. A. 1998 MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Rey R., Lukas-Croisier C., Lasala C. and Bedecarrás P. 2003 AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell Endocrinol. 211, 21–31.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Marí A., Yan Y. L., BreMiller R. A., Wilson C., Cañestro C. and Postlethwait J. H. 2005 Characterization and expression pattern of zebrafish anti-Mullerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Exp. Patterns 5, 655–667.

    Article  Google Scholar 

  • Schmidt D., Ovitt C. E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.-C. et al. 2004 The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131, 933–942.

    Article  CAS  PubMed  Google Scholar 

  • Shen Z. G. and Wang H. P. 2014 Molecular players involved in temperature-dependent sex determination and sex differentiation in teleost fish. Genet. Sel. Evol. 46, 26.

    Article  PubMed  PubMed Central  Google Scholar 

  • Skaar K. S., Nobrega R. H., Magaraki A., Olsen L. C., Schulz R. W. and Male R. 2011 Proteolytically activated, recombinant anti-Müllerian hormone inhibits androgen secretion, proliferation, and differentiation of spermatogonia in adult zebrafish testis organ cultures. Endocrinology 152, 3527–3540.

    Article  CAS  PubMed  Google Scholar 

  • Smith E. K., Guzmán J. M. and Luckenbach J. A. 2013 Molecular cloning, characterization, and sexually dimorphic expression of five major sex differentiation-related genes in a Scorpaeniform fish, sablefish (Anoplopoma fimbria). Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 165, 125–137.

    Article  CAS  Google Scholar 

  • Valenzuela N. 2008 Evolution of the gene network underlying gonadogenesis in turtles with temperature-dependent and genotypic sex determination. Integr. Comp. Biol. 48, 476–485.

    Article  CAS  PubMed  Google Scholar 

  • Vizziano D., Baron D., Randuineau G., Mahe S., Cauty C. and Guiguen Y. 2008 Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation. Biol. Reprod. 78, 939–946.

    Article  CAS  PubMed  Google Scholar 

  • Wang D. D., Zhang G. R., Wei K. J., Ji W., Gardner J. P. A., Yang R. B. and Chen K. C. 2015 Molecular identification and expression of the Foxl2 gene during gonadal sex differentiation in northern snakehead Channa argus. Fish Physiol. Biochem. 41, 1419–1433.

    Article  CAS  PubMed  Google Scholar 

  • Wang D. S., Kobayashi T., Zhou L. Y. and Nagahama Y. 2004 Molecular cloning and gene expression of Foxl2 in the Nile tilapia, Oreochromis niloticus. Biochem. Biophys. Res. Commun. 320, 83–89.

    Article  CAS  PubMed  Google Scholar 

  • Western P. S., Harry J. L., Graves J. A. and Sinclair A. H. 1999 Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev. Dyn. 216, 411–419.

    Article  CAS  PubMed  Google Scholar 

  • Wu J. M., Zhao H. T., Miao Z. G., Chen Y. X., Zhang F. T. and Wang J. W. 2010 Status and conservation of fish resources in the Chishui River. Biodiv. Sci. 18, 162–168.

    Google Scholar 

  • Wu L. 1989 The fishes of Guizhou, pp. 191. Guizhou People’s Press, Guiyang.

    Google Scholar 

  • Yoshinaga N., Shiraishi E., Yamamoto T., Iguchi T., Abe S. and Kitano T. 2004 Sexually dimorphic expression of a teleost homologue of Mullerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem. Biophys. Res. Commun. 322, 508–513.

    Article  CAS  PubMed  Google Scholar 

  • Yue P. Q. 2000 Fauna sinica: Osteichthyes–Cypriniformes III, pp. 327–328. Science Press, Beijing.

    Google Scholar 

  • Zou X. J. 2009 Study on karyotype and genetic diversity in the population of Schizothorax (Racoma) kozlovi. Dissertation of Guizhou University, Guiyang.

    Google Scholar 

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Acknowledgements

Authors are grateful to Z. J. Shu for his help in culturing experimental fish. This work was mainly supported by the National Natural Science Foundation of China (51609255) and the Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (2016JBF0302).

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Authors and Affiliations

  1. Key Laboratory of Freshwater Biodiversity Conservation, Ministry of Agriculture of China, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, Hubei, 430223, People’s Republic of China

    Yongfeng He, Xuge Wang, Xingbing Wu, Yongjiu Zhu & Deguo Yang

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  1. Yongfeng He
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  2. Xuge Wang
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Correspondence to Deguo Yang.

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Corresponding editor: Indrajit Nanda

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He, Y., Wang, X., Wu, X. et al. Expression profiles of amh and foxl2 in Schizothorax kozlovi, and their response to temperature during the early developmental stage. J Genet 97, 127–136 (2018). https://doi.org/10.1007/s12041-018-0889-9

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  • DOI: https://doi.org/10.1007/s12041-018-0889-9

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