Abstract
We studied molecular events and potential mechanisms underlying the process of female-to-male sex transformation in the rice field eel (Monopterus albus), a protogynous hermaphrodite fish in which the gonad is initially a female ovary and transforms into male testes. We cloned and identified a novel gonadal soma derived factor (GSDF), which encodes a member of the transforming growth factor-beta superfamily. gsdf expression was measured in gonads of female, intersex and male with reverse transcription-PCR and gsdf’s role in sex transformation was studied with qPCR, histological analysis and dual-color in situ hybridization assays and compared to other sex-related genes. gsdf was correlated to Sertoli cell differentiation, indicating involvement in testicular differentiation and sex transformation from female to male in this species. A unique expression pattern reveals a potential role of gsdf essential for the sex transformation of rice field eels.
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References
Cutting A, Chue J, Smith CA (2013) Just how conserved is vertebrate sex determination? Dev Dyn 242(4):380–387
Kobayashi Y, Nagahama Y, Nakamura M (2013) Diversity and plasticity of sex determination and differentiation in fishes. Sex Dev 7(1–3):115–125
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
Yang DQ, Cheng F, Ruan GL, Su YB (2008) Relationship between sex reversal, body weight and age of monopterus albus. J. Yangtxe Univ 5(4):45–47
Nagahama Y (2005) Molecular mechanisms of sex determination and gonadal sex differentiation in fish. Fish Physiol Biochem 31(2–3):105–109
Josso N et al (1998) The role of anti-Mullerian hormone in gonadal development. Mol Cell Endocrinol 145(1–2):3–7
da Morais SS et al (1996) Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14(1):62–68
Raymond CS et al (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391(6668):691–695
Smith CA et al (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461(7261):267–271
Pannetier M et al (2006) FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 36(3):399–413
Zhou R et al (2003) Similar gene structure of two Sox9a genes and their expression patterns during gonadal differentiation in a teleost fish, rice field eel (Monopterus albus). Mol Reprod Dev 66(3):211–217
Huang X et al (2005) Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel. Biol Reprod 73(5):1017–1024
Zhang Y et al (2008) Two cytochrome P450 aromatase genes in the hermaphrodite ricefield eel Monopterus albus: mRNA expression during ovarian development and sex change. J Endocrinol 199(2):317–331
Hu Q et al (2014) Molecular cloning and analysis of gonadal expression of Foxl2 in the rice-field eel Monopterus albus. Sci Rep 4:6884
Gao Y et al (2014) Characterization and differential expression patterns of conserved microRNAs and mRNAs in three genders of the rice field eel (Monopterus albus). Sex Dev 8(6):387–398
Hu Q et al (2015) Molecular cloning and characterization of amh and dax1 genes and their expression during sex inversion in rice-field eel Monopterus albus. Sci Rep 5:16667
Yoshinaga N et al (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(2):508–513
Li M et al (2015) A tandem duplicate of anti-Mullerian hormone with a missense SNP on the Y Chromosome is essential for male sex determination in nile tilapia, Oreochromis niloticus. PLoS Genet 11(11):e1005678
Eshel O et al (2014) Identification of male-specific amh duplication, sexually differentially expressed genes and microRNAs at early embryonic development of Nile tilapia (Oreochromis niloticus). BMC Genom 15:774
Hattori RS et al (2012) A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109(8):2955–2959
von Hofsten J, Larsson A, Olsson PE (2005) Novel steroidogenic factor-1 homolog (ff1d) is coexpressed with anti-Mullerian hormone (AMH) in zebrafish. Dev Dyn 233(2):595–604
Sawatari E et al (2007) A novel transforming growth factor-beta 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
Shibata Y et al (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
Kaneko H et al (2015) Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus. Mol Cell Endocrinol 415:87–99
Gautier A, Le Gac F, Lareyre JJ (2011) The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene 472(1–2):7–17
Chen Y et al (2015) Cloning and pattern of gsdf mRNA during gonadal development in the protogynous Epinephelus akaara. Anim Reprod Sci 165:46–55
Horiguchi R et al (2013) Characterization of gonadal soma-derived factor expression during sex change in the protogynous wrasse, Halichoeres trimaculatus. Dev Dyn 242(4):388–399
Chen Y et al (2015) Cloning and expression pattern of gsdf during the first maleness reproductive phase in the protandrous Acanthopagrus latus. Gen Comp Endocrinol 217–218:71–80
Myosho T et al (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191(1):163–170
Sinclair AH et al (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346(6281):240–244
Nanda I et al (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99(18):11778–11783
Matsuda M et al (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417(6888):559–563
Xu H et al (2009) Boule is present in fish and bisexually expressed in adult and embryonic germ cells of medaka. PLoS One 4(6):e6097
Ye D et al (2007) Cloning and characterization of a rice field eel vasa-like gene cDNA and its expression in gonads during natural sex transformation. Biochem Genet 45(3–4):211–224
Ashida H et al (2013) Molecular identification and expression of FOXL2 and DMRT1 genes from willow minnow Gnathopogon caerulescens. Reprod Biol 13(4):317–324
Agrawal R et al (2009) Male-specific expression of Sox9 during gonad development of crocodile and mouse is mediated by alternative splicing of its proline-glutamine-alanine rich domain. FEBS J 276(15):4184–4196
Uhlenhaut NH et al (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139(6):1130–1142
LoNostro F et al (2003) Involvement of the gonadal germinal epithelium during sex reversal and seasonal testicular cycling in the protogynous swamp eel, Synbranchus marmoratus Bloch 1795 (Teleostei, Synbranchidae). J Morphol 257(1):107–126
Guigon CJ et al (2005) Follicular cells acquire sertoli cell characteristics after oocyte loss. Endocrinology 146(7):2992–3004
Matson CK et al (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476(7358):101–104
Masuyama H et al (2012) Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res 20(1):163–176
Zhang X, Guan G, Li M, Zhu F, Liu Q, Naruse K, Herpin A, Nagahama Y, Li J, Hong Y (2015) Autosomal gsdf acts as a male sex initiator in the fish medaka. Sci Rep. in press
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
Acknowledgments
This work was supported by Shanghai University First-class Disciplines Project of Fisheries and a grant to G. Guan by Natural Science Foundation of Shanghai (16ZR1415200). We also thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Authors’ contributions
GG designed the experiments, performed experiments, analyzed the results and wrote the manuscript. ZY carried out experiments, WC and CX performed histological analysis. All authors read and approved the final manuscript.
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Zhu, Y., Wang, C., Chen, X. et al. Identification of gonadal soma-derived factor involvement in Monopterus albus (protogynous rice field eel) sex change. Mol Biol Rep 43, 629–637 (2016). https://doi.org/10.1007/s11033-016-3997-8
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DOI: https://doi.org/10.1007/s11033-016-3997-8