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Identification of Dmrt genes and their up-regulation during gonad transformation in the swamp eel (Monopterus albus)

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Abstract

The swamp eel is a teleost fish with a characteristic of natural sex reversal and an ideal model for vertebrate sexual development. However, underlying molecular mechanisms are poorly understood. We report the identification of five DM (doublesex and mab-3) domain genes in the swamp eel that include Dmrt2, Dmrt2b, Dmrt3, Dmrt4 and Dmrt5, which encode putative proteins of 527, 373, 471, 420 and 448 amino acids, respectively. Phylogenetic tree showed that these genes are clustered into corresponding branches of the DM genes in vertebrates. Southern blot analysis indicated that the Dmrt1–Dmrt3–Dmrt2 genes are tightly linked in a conserved gene cluster. Notably, these Dmrt genes are up-regulated during gonad transformation. Furthermore, mRNA in situ hybridisation showed that Dmrt2, Dmrt3, Dmrt4 and Dmrt5 are expressed in developing germ cells. These results are evidence that the DM genes are involved in sexual differentiation in the swamp eel.

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References

  1. Liu CK (1944) Rudimentary hermaphroditism in the Symbranchoid eel, Monopterus javanesis. Sinensia 15:1–6

    Google Scholar 

  2. Bullough WS (1947) Hermaphroditism in the lower vertebrates. Nature 160:9–11

    Article  CAS  PubMed  Google Scholar 

  3. Cheng H, Guo Y, Yu Q, Zhou R (2003) The rice field eel as a model system for vertebrate sexual development. Cytogenet Genome Res 101:274–277

    Article  CAS  PubMed  Google Scholar 

  4. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351:117–121

    Article  CAS  PubMed  Google Scholar 

  5. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240–244

    Article  CAS  PubMed  Google Scholar 

  6. Berta P, Hawkins JR, Sinclair AH, Taylor A, Griffiths BL, Goodfellow PN, Fellous M (1990) Genetic evidence equating SRY and the testis-determining factor. Nature 348:448–450

    Article  CAS  PubMed  Google Scholar 

  7. Yoshimoto S, Ikeda N, Izutsu Y, Shiba T, Takamatsu N, Ito M (2010) Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system. Development 137:2519–2526

    Article  CAS  PubMed  Google Scholar 

  8. Onesimo R, Orteschi D, Scalzone M, Rossodivita A, Nanni L, Zannoni GF, Marrocco G, Battaglia D, Fundaro C, Neri G (2012) Chromosome 9p deletion syndrome and sex reversal: novel findings and redefinition of the critically deleted regions. Am J Med Genet A 158A:2266–2271

    Article  PubMed  Google Scholar 

  9. Raymond CS, Murphy MW, O’Sullivan MG, Bardwell VJ, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587–2595

    Article  CAS  PubMed  Google Scholar 

  10. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271

    Article  CAS  PubMed  Google Scholar 

  11. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105:2469–2474

    Article  CAS  PubMed  Google Scholar 

  12. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563

    Article  CAS  PubMed  Google Scholar 

  13. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (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 99:11778–11783

    Article  CAS  PubMed  Google Scholar 

  14. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strussmann CA (2012) A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109:2955–2959

    Article  CAS  PubMed  Google Scholar 

  15. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8:e1002798

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191:163–170

    Article  CAS  PubMed  Google Scholar 

  17. Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 22:1423–1428

    Article  CAS  PubMed  Google Scholar 

  18. Kikuchi K, Hamaguchi S (2013) Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn 242:339–353

    Article  CAS  PubMed  Google Scholar 

  19. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695

    Article  CAS  PubMed  Google Scholar 

  20. Hodgkin J (2002) The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: ancestry or aptitude? Genes Dev 16:2322–2326

    Article  CAS  PubMed  Google Scholar 

  21. Kondo M, Froschauer A, Kitano A, Nanda I, Hornung U, Volff JN, Asakawa S, Mitani H, Naruse K, Tanaka M, Schmid M, Shimizu N, Schartl M, Shima A (2002) Molecular cloning and characterization of DMRT genes from the medaka Oryzias latipes and the platyfish Xiphophorus maculatus. Gene 295:213–222

    Article  CAS  PubMed  Google Scholar 

  22. Volff JN, Zarkower D, Bardwell VJ, Schartl M (2003) Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol 57(Suppl 1):S241–S249

    Article  CAS  PubMed  Google Scholar 

  23. Brunner B, Hornung U, Shan Z, Nanda I, Kondo M, Zend-Ajusch E, Haaf T, Ropers HH, Shima A, Schmid M, Kalscheuer VM, Schartl M (2001) Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77:8–17

    Article  CAS  PubMed  Google Scholar 

  24. Ottolenghi C, Fellous M, Barbieri M, McElreavey K (2002) Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics 79:333–343

    Article  CAS  PubMed  Google Scholar 

  25. Kim S, Kettlewell JR, Anderson RC, Bardwell VJ, Zarkower D (2003) Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns 3:77–82

    Article  CAS  PubMed  Google Scholar 

  26. Lints R, Emmons SW (2002) Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev 16:2390–2402

    Article  CAS  PubMed  Google Scholar 

  27. Johnsen H, Andersen O (2012) Sex dimorphic expression of five dmrt genes identified in the Atlantic cod genome. The fish-specific dmrt2b diverged from dmrt2a before the fish whole-genome duplication. Gene 505:221–232

    Article  CAS  PubMed  Google Scholar 

  28. Hong CS, Park BY, Saint-Jeannet JP (2007) The function of Dmrt genes in vertebrate development: it is not just about sex. Dev Biol 310:1–9

    Article  CAS  PubMed  Google Scholar 

  29. Seo KW, Wang Y, Kokubo H, Kettlewell JR, Zarkower DA, Johnson RL (2006) Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev Biol 290:200–210

    Article  CAS  PubMed  Google Scholar 

  30. Lourenco R, Lopes SS, Saude L (2010) Left-right function of dmrt2 genes is not conserved between zebrafish and mouse. PLoS One 5:e14438

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Zhou X, Li Q, Lu H, Chen H, Guo Y, Cheng H, Zhou R (2008) Fish specific duplication of Dmrt2: characterization of zebrafish Dmrt2b. Biochimie 90:878–887

    Article  CAS  PubMed  Google Scholar 

  32. Li Q, Zhou X, Guo Y, Shang X, Chen H, Lu H, Cheng H, Zhou R (2008) Nuclear localization, DNA binding and restricted expression in neural and germ cells of zebrafish Dmrt3. Biol Cell 100:453–463

    Article  CAS  PubMed  Google Scholar 

  33. Balciuniene J, Bardwell VJ, Zarkower D (2006) Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Mol Cell Biol 26:8984–8991

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Huang X, Hong CS, O’Donnell M, Saint-Jeannet JP (2005) The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci USA 102:11349–11354

    Article  CAS  PubMed  Google Scholar 

  35. Guo Y, Li Q, Gao S, Zhou X, He Y, Shang X, Cheng H, Zhou R (2004) Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem Biophys Res Commun 324:569–575

    Article  CAS  PubMed  Google Scholar 

  36. Parlier D, Moers V, Van Campenhout C, Preillon J, Leclere L, Saulnier A, Sirakov M, Busengdal H, Kricha S, Marine JC, Rentzsch F, Bellefroid EJ (2013) The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis. Dev Biol 373:39–52

    Article  CAS  PubMed  Google Scholar 

  37. Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R (2005) Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun 330:950–957

    Article  CAS  PubMed  Google Scholar 

  38. Huang X, Guo Y, Shui Y, Gao S, Yu H, Cheng H, Zhou R (2005) Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel. Biol Reprod 73:1017–1024

    Article  CAS  PubMed  Google Scholar 

  39. Jang S, Zhou F, Xia L, Zhao W, Cheng H, Zhou R (2006) Construction of a BAC library and identification of Dmrt1 gene of the rice field eel, Monopterus albus. Biochem Biophys Res Commun 348:775–780

    Article  CAS  PubMed  Google Scholar 

  40. El-Mogharbel N, Wakefield M, Deakin JE, Tsend-Ayush E, Grutzner F, Alsop A, Ezaz T, Marshall Graves JA (2007) DMRT gene cluster analysis in the platypus: new insights into genomic organization and regulatory regions. Genomics 89:10–21

    Article  CAS  PubMed  Google Scholar 

  41. Meng A, Moore B, Tang H, Yuan B, Lin S (1999) A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development 126:1259–1268

    CAS  PubMed  Google Scholar 

  42. Herpin A, Schartl M (2011) Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 278:1010–1019

    Article  CAS  PubMed  Google Scholar 

  43. Lei N, Hornbaker KI, Rice DA, Karpova T, Agbor VA, Heckert LL (2007) Sex-specific differences in mouse DMRT1 expression are both cell type- and stage-dependent during gonad development. Biol Reprod 77:466–475

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China, the National Key Basic Research project, National Key Technologies R&D Program and Hubei Province Science and Technology project. Authors thank five reviewers for their comments and suggestions.

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The authors declare that there is no conflict of interest.

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Authors and Affiliations

  1. Department of Genetics and Center for Developmental Biology, College of Life Sciences, Wuhan University, Wuhan, 430072, People’s Republic of China

    Yue Sheng, Bo Chen, Liao Zhang, Majing Luo, Hanhua Cheng & Rongjia Zhou

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  1. Yue Sheng
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  2. Bo Chen
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  3. Liao Zhang
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Correspondence to Hanhua Cheng or Rongjia Zhou.

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Sheng, Y., Chen, B., Zhang, L. et al. Identification of Dmrt genes and their up-regulation during gonad transformation in the swamp eel (Monopterus albus). Mol Biol Rep 41, 1237–1245 (2014). https://doi.org/10.1007/s11033-013-2968-6

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  • DOI: https://doi.org/10.1007/s11033-013-2968-6

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