Characterization of the Dmrt1 gene in the black rockfish Sebastes schlegeli revealed a remarkable sex-dimorphic expression

Fish Physiology and Biochemistry

Volumn 40, Issue 4, 2014, Pages 1263-1274

  Ma, Liman ^a   Wang, Wenji ^a   Yang, Xiao ^a   Jiang, Jiajun ^a   Song, Huayu ^a   Jiang, Haibin ^b   Zhang, Quanqi ^a   Qi, Jie ^a  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b Shandong Marine Fisheries Research Institute   (China)

Author keywords

Black rockfish; Dmrt1; Promoter analysis; Sebastes schlegeli; Sex dimorphic expression

Indexed keywords

INVERTEBRATA; SEBASTES MELANOPS; SEBASTES SCHLEGELI; TETRAPODA; VERTEBRATA;

COMPLEMENTARY DNA; DMRT1 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE STRUCTURE; GENETICS; GERM CELL; HUMAN; IN SITU HYBRIDIZATION; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PERCIFORMES; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT;

ANIMALS; BASE SEQUENCE; DNA, COMPLEMENTARY; GENE COMPONENTS; GENE EXPRESSION REGULATION; GERM CELLS; HUMANS; IN SITU HYBRIDIZATION; MALE; MOLECULAR SEQUENCE DATA; PERCIFORMES; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS;

EID: 84903631196     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-014-9921-z     Document Type: Article

References (46)

1. Aoyama S, Shibata K, Tokunaga S, Takase M, Matsui K, Nakamura M (2003) Expression of Dmrt1 protein in developing and in sex-reversed gonads of amphibians. Cytogenet Genome Res 101(3-4): 295-301.
2. Boyer A, Dornan S, Daneau I, Lussier J, Silversides DW (2002) Conservation of the function of DMRT1 regulatory sequences in mammalian sex differentiation. Genesis 34: 236-243.
3. Brunner B, Hornung U, Shan Z, Nanda I, Kondo M, Zend-Ajusch E, Haaf T, Ropers H-H, Shima A, Schmid M (2001) Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77(1): 8-17.
4. Cao J, Chen J, Wu T, Gan X, Luo Y (2010) Molecular cloning and sexually dimorphic expression of DMRT4 gene in Oreochromis aureus. Mol Biol Rep 37(6): 2781-2788.
5. Cao M, Duan J, Cheng N, Zhong X, Wang Z, Hu W, Zhao H (2012) Sexually dimorphic and ontogenetic expression of dmrt1, cyp19a1a and cyp19a1b in Gobiocypris rarus. Comp Biochem Physiol A: Mol Integr Physiol 162(4): 303-309.
6. Erdman SE, Burtis KC (1993) The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 12(2): 527.
7. Gao S, Zhang T, Zhou X, Zhao Y, Li Q, Guo Y, Cheng H, Zhou R (2005) Molecular cloning, expression of Sox5 and its down-regulation of Dmrt1 transcription in Zebrafish. J Exp Zool Part B Mol Dev Evol 304(5): 476-483.
8. Guan G, Kobayashi T, Nagahama Y (2000) Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 272(3): 662-666.
9. 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(2): 569-575.
10. 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(3): 950-957.
11. He C-L, Du J-L, Wu G-C, Lee Y-H, Sun L-T, Chang C-F (2003) Differential Dmrt1 transcripts in gonads of the protandrous black porgy, Acanthopagrus schlegeli. Cytogenet Genome Res 101(3-4): 309-313.
12. Hong C-S, Park B-Y, Saint-Jeannet J-P (2007) The function of Dmrt genes in vertebrate development: it is not just about sex. Dev Biol 310(1): 1-9.
13. Jeong H-B, Park J-G, Park Y-J, Takemura A, Hur S-P, Lee Y-D, Kim S-J (2009) Isolation and characterization of DMRT1 and its putative regulatory region in the protogynous wrasse, Halichoeres tenuispinis. Gene 438(1): 8-16.
14. Jo P, An K, Kim N, Choi Y, Cho S, Min B, Lim H, Choi C (2007) Induced expression of doublesex-and mab-3-related transcription factor-1 (DMRT-1) mRNA by testosterone in the olive flounder, Paralichthys olivaceus ovary. J Aquac 20: 199-202.
15. Johnsen H, Seppola M, Torgersen JS, Delghandi M, Andersen Ø (2010) Sexually dimorphic expression of dmrt1 in immature and mature Atlantic cod (Gadus morhua L.). Comp Biochem Physiol B: Biochem Mol Biol 156(3): 197-205.
16. 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(1): 77-82.
17. Kim S, Bardwell VJ, Zarkower D (2007) Cell type-autonomous and non-autonomous requirements for Dmrt1 in postnatal testis differentiation. Dev Biol 307(2): 314-327.
18. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y (2004) Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231(3): 518-526.
19. Kobayashi T, Kajiura-Kobayashi H, Guan G, Nagahama Y (2008) Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish Nile tilapia (Oreochromis niloticus). Dev Dyn 237(1): 297-306.
20. Kondo M, Froschauer A, Kitano A, Nanda I, Hornung U, Volff J-N, 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(2): 213-222.
21. Leet J, Lesteberg K, Schoenfuss H, Olmstead A, Amberg J, Ankley G, Sepúlveda M (2013) Sex-specific gonadal and gene expression changes throughout development in fathead minnow. Sex Dev. doi: 10. 1159/000353877.
22. Lei N, Heckert LL (2004) Gata4 regulates testis expression of Dmrt1. Mol Cell Biol 24(1): 377-388.
23. Ma L, Wang W, Liu C, Yu H, Wang Z, Wang X, Qi J, Zhang Q (2013) Selection of reference genes for reverse transcription quantitative real-time PCR normalization in black rockfish (Sebastes schlegeli). Mar Genomics 11: 67-73.
24. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre J-J, Bernot A, Laudet V, Guiguen Y (2000) DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 1493(1): 180-187.
25. Matsushita Y, Oshima Y, Nakamura M (2007) Expression of DMRT genes in the gonads of Rana rugosa during sex determination. Zoolog Sci 24(1): 95-99.
26. Moniot B, Berta P, Scherer G, Südbeck P, Poulat F (2000) Male specific expression suggests role of DMRT1 in human sex determination. Mech Dev 91(1): 323-325.
27. Murdock C, Wibbels T (2003) Expression of Dmrt1 in a turtle with temperature-dependent sex determination. Cytogenet Genome Res 101(3-4): 302-308.
28. Omoto N, Koya Y, Chin B, Yamashita Y, Nakagawa M, Noda T (2010) Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish (Sebastes schlegeli). Ichthyol Res 57(2): 133-138.
29. 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(6668): 691-695.
30. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D (1999a) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215(2): 208-220.
31. Raymond CS, Parker ED, Kettlewell JR, Brown LG, Page DC, Kusz K, Jaruzelska J, Reinberg Y, Flejter WL, Bardwell VJ (1999b) A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8(6): 989-996.
32. 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(20): 2587-2595.
33. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4): 406-425.
34. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T (2000) Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Genome Res 89(3-4): 252-257.
35. Shibata K, Takase M, Nakamura M (2002) The Dmrt1 expression in sex-reversed gonads of amphibians. Gen Comp Endocrinol 127(3): 232-241.
36. 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(7261): 267-271.
37. Smith EK, Guzmán JM, Luckenbach JA (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 Part B 165: 125-137.
38. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24): 4876-4882.
39. Veith A-M, Schäfer M, Klüver N, Schmidt C, Schultheis C, Schartl M, Winkler C, Volff J-N (2006) Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish 3(3): 325-337.
40. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79(6): 1111-1120.
41. Wang D-S, Zhou L-Y, Kobayashi T, Matsuda M, Shibata Y, Sakai F, Nagahama Y (2010) Doublesex-and Mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology 151(3): 1331-1340.
42. Wen A, You F, Tan X, Sun P, Ni J, Zhang Y, Xu D, Wu Z, Xu Y, Zhang P (2009) Expression pattern of dmrt4 from olive flounder (Paralichthys olivaceus) in adult gonads and during embryogenesis. Fish Physiol Biochem 35(3): 421-433.
43. Wu G-C, Chiu P-C, Lin C-J, Lyu Y-S, Lan D-S, Chang C-F (2011) Testicular dmrt1 is involved in the sexual fate of the ovotestis in the protandrous black porgy. Biol Reprod 86(2): 1-11.
44. Yamaguchi A, Lee KH, Fujimoto H, Kadomura K, Yasumoto S, Matsuyama M (2006) Expression of the DMRT gene and its roles in early gonadal development of the Japanese pufferfish Takifugu rubripes. Comp Biochem Physiol D: Genomics Proteomics 1(1): 59-68.
45. Ying M, Chen B, Tian Y, Hou Y, Li Q, Shang X, Sun J, Cheng H, Zhou R (2007) Nuclear import of human sexual regulator DMRT1 is mediated by importin-β. Biochim Biophys Acta 1773(6): 804-813.
46. Zhou Q, Shao M, Qin Z, Kyoung HK, Zhang Z (2010) Cloning, characterization, and expression analysis of the DEAD-box family genes, Fc-vasa and Fc-PL10a, in Chinese shrimp (Fenneropenaeus chinensis). Chin J Oceanol Limnol 28(1): 37-45.