Characterization of SOX3 Gene in an Ovoviviparous Teleost, Black Rockfish(Sebastes schlegeli)
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摘要
Evolutionary evidence suggests that Sox3, a member of the high-mobility-group(HMG) family of transcription factors, is an ancestral precursor of Sry and is involved in sex determination similar to Sry. However, there is limited information regarding the SOX3 gene of the black rockfish(Sebastes schlegeli). In this study, we first isolated SOX3 gene from the gonads of S. schlegeli by homology cloning. The full-length of S. schlegeli SOX3(SsSOX3) c DNA was 1386 bp, comprising a 906-bp open reading frame, which encodes a peptide showing 93.6% and 93.9% homology with the Sox3 proteins of Epinephelus coioides and Oryzias latipe, respectively. Comparison of the cDNA sequence of the Ss SOX3 gene with the corresponding genomic DNA fragment revealed that the SsSOX3 gene consists of a single exon. Phylogenetic analysis demonstrated the evolutionary relationship of Ss SOX3 with other known SOXB1 genes in fish and tetrapods. The promoter region contains binding sites of several transcriptional factors that might participate in the regulation of Ss SOX3 expression. Quantitative real-time PCR analysis indicated that SsSOX3 was expressed in all the investigated larval developmental stages from 1 to 35 days after birth and the level of expression gradually decreased as the development proceeded. SsSOX3 exhibited sexually dimorphic expression in adult gonads, with high expression in the ovary but low expression in the testis. In situ hybridization revealed that SsSOX3 was strongly expressed in oocytes and follicular cells of ovaries but slightly expressed in germ cells of testicular tissues. Therefore, this study suggests that Ss SOX3 plays an important role in oogenesis and ovary differentiation in S. schlegeli.
Evolutionary evidence suggests that Sox3, a member of the high-mobility-group(HMG) family of transcription factors, is an ancestral precursor of Sry and is involved in sex determination similar to Sry. However, there is limited information regarding the SOX3 gene of the black rockfish(Sebastes schlegeli). In this study, we first isolated SOX3 gene from the gonads of S. schlegeli by homology cloning. The full-length of S. schlegeli SOX3(SsSOX3) c DNA was 1386 bp, comprising a 906-bp open reading frame, which encodes a peptide showing 93.6% and 93.9% homology with the Sox3 proteins of Epinephelus coioides and Oryzias latipe, respectively. Comparison of the cDNA sequence of the Ss SOX3 gene with the corresponding genomic DNA fragment revealed that the SsSOX3 gene consists of a single exon. Phylogenetic analysis demonstrated the evolutionary relationship of Ss SOX3 with other known SOXB1 genes in fish and tetrapods. The promoter region contains binding sites of several transcriptional factors that might participate in the regulation of Ss SOX3 expression. Quantitative real-time PCR analysis indicated that SsSOX3 was expressed in all the investigated larval developmental stages from 1 to 35 days after birth and the level of expression gradually decreased as the development proceeded. SsSOX3 exhibited sexually dimorphic expression in adult gonads, with high expression in the ovary but low expression in the testis. In situ hybridization revealed that SsSOX3 was strongly expressed in oocytes and follicular cells of ovaries but slightly expressed in germ cells of testicular tissues. Therefore, this study suggests that Ss SOX3 plays an important role in oogenesis and ovary differentiation in S. schlegeli.
Evolutionary evidence suggests that Sox3, a member of the high-mobility-group(HMG) family of transcription factors, is an ancestral precursor of Sry and is involved in sex determination similar to Sry. However, there is limited information regarding the SOX3 gene of the black rockfish(Sebastes schlegeli). In this study, we first isolated SOX3 gene from the gonads of S. schlegeli by homology cloning. The full-length of S. schlegeli SOX3(SsSOX3) c DNA was 1386 bp, comprising a 906-bp open reading frame, which encodes a peptide showing 93.6% and 93.9% homology with the Sox3 proteins of Epinephelus coioides and Oryzias latipe, respectively. Comparison of the cDNA sequence of the Ss SOX3 gene with the corresponding genomic DNA fragment revealed that the SsSOX3 gene consists of a single exon. Phylogenetic analysis demonstrated the evolutionary relationship of Ss SOX3 with other known SOXB1 genes in fish and tetrapods. The promoter region contains binding sites of several transcriptional factors that might participate in the regulation of Ss SOX3 expression. Quantitative real-time PCR analysis indicated that SsSOX3 was expressed in all the investigated larval developmental stages from 1 to 35 days after birth and the level of expression gradually decreased as the development proceeded. SsSOX3 exhibited sexually dimorphic expression in adult gonads, with high expression in the ovary but low expression in the testis. In situ hybridization revealed that SsSOX3 was strongly expressed in oocytes and follicular cells of ovaries but slightly expressed in germ cells of testicular tissues. Therefore, this study suggests that Ss SOX3 plays an important role in oogenesis and ovary differentiation in S. schlegeli.
引文
Bergstrom,D.E.,Young,M.,Albrecht,K.H.,and Eicher,E.M.,2000.Related function of mouse SOX3,SOX9,and SRYHMG domains assayed by male sex determination.Genesis,28(3-4):111-124.
Bowles,J.,Schepers,G.,and Koopman,P.,2000.Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators.Developmental Biology,227(2):239-255.
Cheah,P.S.,and Thomas,P.Q.,2015.SOX3 expression in the glial system of the developing and adult mouse cerebellum.Springerplus,4:400.
Dee,C.T.,Hirst,C.S.,Shih,Y.H.,Tripathi,V.B.,Patient,R.K.,and Scotting,P.J.,2008.Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm.Developmental Biology,320(1):289-301.
Feng,J.R.,Liu,L.M.,Jiang,H.B.,Wang,M.J.,and Du,R.B.,2014.Histological observation of germ cell development and discovery of spermatophores in ovoviviparous black rockfish(Sebastes schlegeli Hilgendorf)in reproductive season.Journal of Ocean University of China,13(5):830-836.
Foster,J.W.,and Graves,J.A.,1994.An SRY-related sequence on the marsupial X chromosome:Implications for the evolution of the mammalian testis-determining gene.Proceedings of the National Academy of Sciences of the United States of America,91(5):1927-1931.
Gao,J.,Li,P.,Zhang,W.,Wang,Z.,Wang,X.,and Zhang,Q.,2015.Molecular cloning,promoter analysis and expression profiles of the sox3 gene in Japanese flounder,Paralichthys olivaceus.International Journal of Molecular Sciences,16(11):27931-27944.
Graves,J.A.,1998.Evolution of the mammalian Y chromosome and sex-determining genes.Journal of Experimental Zoology,281(5):472-481.
Grujicic,N.K.,Mojsin,M.,Krstic,A.,and Stevanovic,M.,2005.Functional characterization of the human SOX3 promoter:Identification of transcription factors implicated in basal promoter activity.Gene,344:287-297.
Jeng,S.R.,Wu,G.C.,Yueh,W.S.,Kuo,S.F.,Dufour,S.,and Chang,C.F.,2017.Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel.General and Comparative Endocrinology,DOI:10.1016/j.ygcen.2017.07.031.
Kobayashi,T.,Kajiura-Kobayashi,H.,Guan,G.,and 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).Developmental Dynamics,237(1):297-306.
Koopman,P.,Gubbay,J.,Vivian,N.,Goodfellow,P.,and LovellBadge,R.,1991.Male development of chromosomally female mice transgenic for Sry.Nature,351(6322):117-121.
Koyano,S.,Ito,M.,Takamatsu,N.,Takiguchi,S.,and Shiba,T.,1997.The Xenopus Sox3 gene expressed in oocytes of early stages.Gene,188(1):101-107.
Lee,K.,Tan,J.,Morris,M.B.,Rizzoti,K.,Hughes,J.,Cheah,P.S.,Felquer,F.,Liu,X.,Piltz,S.,Lovell-Badge,R.,and Thomas,P.Q.,2012.Congenital hydrocephalus and abnormal subcommissural organ development in Sox3 transgenic mice.PLo S One,7(1):e29041.
Ma,L.,Wang,W.,Liu,C.,Yu,H.,Wang,Z.,Wang,X.,Qi,J.,and Zhang,Q.,2013.Selection of reference genes for reverse transcription quantitative real-time PCR normalization in black rockfish(Sebastes schlegeli).Marine Genomics,11:67-73.
Ma,L.,Wang,W.,Yang,X.,Jiang,J.,Song,H.,Jiang,H.,Zhang,Q.,and Qi,J.,2014.Characterization of the Dmrt1 gene in the black rockfish Sebastes schlegeli revealed a remarkable sexdimorphic expression.Fish Physiology and Biochemistry,40(4):1263-1274.
Mojsin,M.,and Stevanovic,M.,2009.PBX1 and MEIS1 upregulate SOX3 gene expression by direct interaction with a consensus binding site within the basal promoter region.Biochemical Journal,425(1):107-116.
Navarro-Martín,L.,Galay-Burgos,M.,Sweeney,G.,and Piferrer,F.,2009.Different sox17 transcripts during sex differentiation in sea bass,Dicentrarchus labrax.Molecular and Cellular Endocrinology,299(2):240-251.
Omoto,N.,Koya,Y.,Chin,B.,Yamashita,Y.,Nakagawa,M.,and Noda,T.,2009.Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish(Sebastes schlegeli).Ichthyological Research,57(2):133-138.
Rajakumar,A.,and Senthilkumaran,B.,2016.Sox3 binds to11beta-hydroxysteroid dehydrogenase gene promoter suggesting transcriptional interaction in catfish.Journal of Steroid Biochemistry and Molecular Biology,158:90-103.
Raverot,G.,Weiss,J.,Park,S.Y.,Hurley,L.,and Jameson,J.L.,2005.Sox3 expression in undifferentiated spermatogonia is required for the progression of spermatogenesis.Developmental Biology,283(1):215-225.
Rizzoti,K.,Brunelli,S.,Carmignac,D.,Thomas,P.Q.,Robinson,I.C.,and Lovell-Badge,R.,2004.SOX3 is required during the formation of the hypothalamo-pituitary axis.Nature Genetics,36(3):247-255.
Rodríguez-Marí,A.,Yan,Y.L.,BreMiller,R.A.,Wilson,C.,Canestro,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 Expression Patterns,5(5):655-667.
Saitou,N.,and Nei,M.,1987.The neighbor-joining method:Anew method for reconstructing phylogenetic trees.Molecular Biology and Evolution,4(4):406-425.
Sambrook,J.,and Russell,D.W.,2016.Molecular Cloning:ALaboratory Manual.Huang,P.T.,trans.,Science Press,Beijing,1661-1681(in Chinese).
Shi,D.,Wen,H.S.,and Yang,Y.P.,2011.The annual change of ovarian development in female Sebastes schlegeli.Periodical of Ocean University of China,41(9):25-30(in Chinese with English abstract).
Shin,H.S.,An,K.W.,Park,M.S.,Jeong,M.H.,and Choi,C.Y.,2009.Quantitative mRNA expression of sox3 and DMRT1during sex reversal,and expression profiles after GnRHa administration in black porgy,Acanthopagrus schlegeli.Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,154(1):150-156.
Sinclair,A.H.,Berta,P.,Palmer,M.S.,Hawkins,J.R.,Griffiths,B.L.,Smith,M.J.,Foster,J.W.,Frischauf,A.M.,LovellBadge,R.,and Goodfellow,P.N.,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.
Stevanovic,M.,Lovell-Badge,R.,Collignon,J.,and Goodfellow,P.N.,1993.SOX3 is an X-linked gene related to SRY.Human Molecular Genetics,2(12):2013-2018.
Takehana,Y.,Matsuda,M.,Myosho,T.,Suster,M.L.,Kawakami,K.,Shin,I.T.,Kohara,Y.,Kuroki,Y.,Toyoda,A.,Fujiyama,A.,Hamaguchi,S.,Sakaizumi,M.,and Naruse,K.,2014.Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena.Nature Communications,5:4157.
Tamura,K.,Peterson,D.,Peterson,N.,Stecher,G.,Nei,M.,and Kumar,S.,2011.MEGA5:Molecular evolutionary genetics analysis using maximum likelihood,evolutionary distance,and maximum parsimony methods.Molecular Biology and Evolution,28(10):2731-2739.
Thompson,J.D.,Gibson,T.J.,Plewniak,F.,Jeanmougin,F.,and Higgins,D.G.,1997.The CLUSTAL_X windows interface:Flexible strategies for multiple sequence alignment aided by quality analysis tools.Nucleic Acids Research,25(24):4876-4882.
Uchikawa,M.,Kamachi,Y.,and Kondoh,H.,1999.Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors:Their expression during embryonic organogenesis of the chicken.Mechanisms of Development,84(1-2):103-120.
Wang,R.,Cheng,H.H.,Xia,L.X.,Guo,Y.Q.,Huang,X.,and Zhou,R.J.,2003.Molecular cloning and expression of Sox17in gonads during sex reversal in the rice field eel,a teleost fish with a characteristic of natural sex transformation.Biochemical and Biophysical Research Communications,303(2):452-457.
Weiss,J.,Meeks,J.J.,Hurley,L.,Raverot,G.,Frassetto,A.,and Jameson,J.L.,2003.Sox3 is required for gonadal function,but not sex determination,in males and females.Molecular and Cellular Biology,23(22):8084-8091.
Wright,E.M.,Snopek,B.,and Koopman,P.,1993.Seven new members of the Sox gene family expressed during mouse development.Nucleic Acids Research,21(3):744.
Wu,D.Y.,and Yao,Z.,2005.Isolation and characterization of the murine Nanog gene promoter.Cell Research,15(5):317-324.
Wu,X.,Wang,Z.,Jiang,J.,Gao,J.,Wang,J.,Zhou,X.,and Zhang,Q.,2014.Cloning,expression promoter analysis of vasa gene in Japanese flounder(Paralichthys olivaceus).Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,167:41-50.
Xia,X.,Huo,W.,Wan,R.,Zhang,L.,Xia,X.,and Chang,Z.,2017.Molecular cloning and expression analysis of Sox3during gonad and embryonic development in Misgurnus anguillicaudatus.International Journal of Developmental Biology,61(8-9):565-570.
Yao,B.,Zhou,L.,and Gui,J.F.,2003.Studies on cDNA cloning and temporal and spatial expression of sox3 gene ingrouper Epinephelus coioides.High Technology Letters,13(5):74-81(in Chinese with English abstract).
Yao,B.,Zhou,L.,Wang,Y.,Xia,W.,and Gui,J.F.,2007.Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish.Journal of Experimental Zoology.Part A:Ecological Genetics and Physiology,307(4):207-219.
Zhang,L.,Lin,D.,Zhang,Y.,Ma,G.,and Zhang,W.,2008.Ahomologue of sox11 predominantly expressed in the ovary of the orange-spotted grouper Epinephelus coioides.Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,149(2):345-353.
Zhou,Q.,Shao,M.,Qin,Z.,Kyoung,H.K.,and Zhang,Z.,2010.Cloning,characterization,and expression analysis of the DEAD-box family genes,Fc-vasa and Fc-PL10a,in Chinese shrimp(Fenneropenaeus chinensis).Chinese Journal of Oceanology and Limnology,28(1):37-45.
Bowles,J.,Schepers,G.,and Koopman,P.,2000.Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators.Developmental Biology,227(2):239-255.
Cheah,P.S.,and Thomas,P.Q.,2015.SOX3 expression in the glial system of the developing and adult mouse cerebellum.Springerplus,4:400.
Dee,C.T.,Hirst,C.S.,Shih,Y.H.,Tripathi,V.B.,Patient,R.K.,and Scotting,P.J.,2008.Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm.Developmental Biology,320(1):289-301.
Feng,J.R.,Liu,L.M.,Jiang,H.B.,Wang,M.J.,and Du,R.B.,2014.Histological observation of germ cell development and discovery of spermatophores in ovoviviparous black rockfish(Sebastes schlegeli Hilgendorf)in reproductive season.Journal of Ocean University of China,13(5):830-836.
Foster,J.W.,and Graves,J.A.,1994.An SRY-related sequence on the marsupial X chromosome:Implications for the evolution of the mammalian testis-determining gene.Proceedings of the National Academy of Sciences of the United States of America,91(5):1927-1931.
Gao,J.,Li,P.,Zhang,W.,Wang,Z.,Wang,X.,and Zhang,Q.,2015.Molecular cloning,promoter analysis and expression profiles of the sox3 gene in Japanese flounder,Paralichthys olivaceus.International Journal of Molecular Sciences,16(11):27931-27944.
Graves,J.A.,1998.Evolution of the mammalian Y chromosome and sex-determining genes.Journal of Experimental Zoology,281(5):472-481.
Grujicic,N.K.,Mojsin,M.,Krstic,A.,and Stevanovic,M.,2005.Functional characterization of the human SOX3 promoter:Identification of transcription factors implicated in basal promoter activity.Gene,344:287-297.
Jeng,S.R.,Wu,G.C.,Yueh,W.S.,Kuo,S.F.,Dufour,S.,and Chang,C.F.,2017.Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel.General and Comparative Endocrinology,DOI:10.1016/j.ygcen.2017.07.031.
Kobayashi,T.,Kajiura-Kobayashi,H.,Guan,G.,and 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).Developmental Dynamics,237(1):297-306.
Koopman,P.,Gubbay,J.,Vivian,N.,Goodfellow,P.,and LovellBadge,R.,1991.Male development of chromosomally female mice transgenic for Sry.Nature,351(6322):117-121.
Koyano,S.,Ito,M.,Takamatsu,N.,Takiguchi,S.,and Shiba,T.,1997.The Xenopus Sox3 gene expressed in oocytes of early stages.Gene,188(1):101-107.
Lee,K.,Tan,J.,Morris,M.B.,Rizzoti,K.,Hughes,J.,Cheah,P.S.,Felquer,F.,Liu,X.,Piltz,S.,Lovell-Badge,R.,and Thomas,P.Q.,2012.Congenital hydrocephalus and abnormal subcommissural organ development in Sox3 transgenic mice.PLo S One,7(1):e29041.
Ma,L.,Wang,W.,Liu,C.,Yu,H.,Wang,Z.,Wang,X.,Qi,J.,and Zhang,Q.,2013.Selection of reference genes for reverse transcription quantitative real-time PCR normalization in black rockfish(Sebastes schlegeli).Marine Genomics,11:67-73.
Ma,L.,Wang,W.,Yang,X.,Jiang,J.,Song,H.,Jiang,H.,Zhang,Q.,and Qi,J.,2014.Characterization of the Dmrt1 gene in the black rockfish Sebastes schlegeli revealed a remarkable sexdimorphic expression.Fish Physiology and Biochemistry,40(4):1263-1274.
Mojsin,M.,and Stevanovic,M.,2009.PBX1 and MEIS1 upregulate SOX3 gene expression by direct interaction with a consensus binding site within the basal promoter region.Biochemical Journal,425(1):107-116.
Navarro-Martín,L.,Galay-Burgos,M.,Sweeney,G.,and Piferrer,F.,2009.Different sox17 transcripts during sex differentiation in sea bass,Dicentrarchus labrax.Molecular and Cellular Endocrinology,299(2):240-251.
Omoto,N.,Koya,Y.,Chin,B.,Yamashita,Y.,Nakagawa,M.,and Noda,T.,2009.Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish(Sebastes schlegeli).Ichthyological Research,57(2):133-138.
Rajakumar,A.,and Senthilkumaran,B.,2016.Sox3 binds to11beta-hydroxysteroid dehydrogenase gene promoter suggesting transcriptional interaction in catfish.Journal of Steroid Biochemistry and Molecular Biology,158:90-103.
Raverot,G.,Weiss,J.,Park,S.Y.,Hurley,L.,and Jameson,J.L.,2005.Sox3 expression in undifferentiated spermatogonia is required for the progression of spermatogenesis.Developmental Biology,283(1):215-225.
Rizzoti,K.,Brunelli,S.,Carmignac,D.,Thomas,P.Q.,Robinson,I.C.,and Lovell-Badge,R.,2004.SOX3 is required during the formation of the hypothalamo-pituitary axis.Nature Genetics,36(3):247-255.
Rodríguez-Marí,A.,Yan,Y.L.,BreMiller,R.A.,Wilson,C.,Canestro,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 Expression Patterns,5(5):655-667.
Saitou,N.,and Nei,M.,1987.The neighbor-joining method:Anew method for reconstructing phylogenetic trees.Molecular Biology and Evolution,4(4):406-425.
Sambrook,J.,and Russell,D.W.,2016.Molecular Cloning:ALaboratory Manual.Huang,P.T.,trans.,Science Press,Beijing,1661-1681(in Chinese).
Shi,D.,Wen,H.S.,and Yang,Y.P.,2011.The annual change of ovarian development in female Sebastes schlegeli.Periodical of Ocean University of China,41(9):25-30(in Chinese with English abstract).
Shin,H.S.,An,K.W.,Park,M.S.,Jeong,M.H.,and Choi,C.Y.,2009.Quantitative mRNA expression of sox3 and DMRT1during sex reversal,and expression profiles after GnRHa administration in black porgy,Acanthopagrus schlegeli.Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,154(1):150-156.
Sinclair,A.H.,Berta,P.,Palmer,M.S.,Hawkins,J.R.,Griffiths,B.L.,Smith,M.J.,Foster,J.W.,Frischauf,A.M.,LovellBadge,R.,and Goodfellow,P.N.,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.
Stevanovic,M.,Lovell-Badge,R.,Collignon,J.,and Goodfellow,P.N.,1993.SOX3 is an X-linked gene related to SRY.Human Molecular Genetics,2(12):2013-2018.
Takehana,Y.,Matsuda,M.,Myosho,T.,Suster,M.L.,Kawakami,K.,Shin,I.T.,Kohara,Y.,Kuroki,Y.,Toyoda,A.,Fujiyama,A.,Hamaguchi,S.,Sakaizumi,M.,and Naruse,K.,2014.Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena.Nature Communications,5:4157.
Tamura,K.,Peterson,D.,Peterson,N.,Stecher,G.,Nei,M.,and Kumar,S.,2011.MEGA5:Molecular evolutionary genetics analysis using maximum likelihood,evolutionary distance,and maximum parsimony methods.Molecular Biology and Evolution,28(10):2731-2739.
Thompson,J.D.,Gibson,T.J.,Plewniak,F.,Jeanmougin,F.,and Higgins,D.G.,1997.The CLUSTAL_X windows interface:Flexible strategies for multiple sequence alignment aided by quality analysis tools.Nucleic Acids Research,25(24):4876-4882.
Uchikawa,M.,Kamachi,Y.,and Kondoh,H.,1999.Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors:Their expression during embryonic organogenesis of the chicken.Mechanisms of Development,84(1-2):103-120.
Wang,R.,Cheng,H.H.,Xia,L.X.,Guo,Y.Q.,Huang,X.,and Zhou,R.J.,2003.Molecular cloning and expression of Sox17in gonads during sex reversal in the rice field eel,a teleost fish with a characteristic of natural sex transformation.Biochemical and Biophysical Research Communications,303(2):452-457.
Weiss,J.,Meeks,J.J.,Hurley,L.,Raverot,G.,Frassetto,A.,and Jameson,J.L.,2003.Sox3 is required for gonadal function,but not sex determination,in males and females.Molecular and Cellular Biology,23(22):8084-8091.
Wright,E.M.,Snopek,B.,and Koopman,P.,1993.Seven new members of the Sox gene family expressed during mouse development.Nucleic Acids Research,21(3):744.
Wu,D.Y.,and Yao,Z.,2005.Isolation and characterization of the murine Nanog gene promoter.Cell Research,15(5):317-324.
Wu,X.,Wang,Z.,Jiang,J.,Gao,J.,Wang,J.,Zhou,X.,and Zhang,Q.,2014.Cloning,expression promoter analysis of vasa gene in Japanese flounder(Paralichthys olivaceus).Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,167:41-50.
Xia,X.,Huo,W.,Wan,R.,Zhang,L.,Xia,X.,and Chang,Z.,2017.Molecular cloning and expression analysis of Sox3during gonad and embryonic development in Misgurnus anguillicaudatus.International Journal of Developmental Biology,61(8-9):565-570.
Yao,B.,Zhou,L.,and Gui,J.F.,2003.Studies on cDNA cloning and temporal and spatial expression of sox3 gene ingrouper Epinephelus coioides.High Technology Letters,13(5):74-81(in Chinese with English abstract).
Yao,B.,Zhou,L.,Wang,Y.,Xia,W.,and Gui,J.F.,2007.Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish.Journal of Experimental Zoology.Part A:Ecological Genetics and Physiology,307(4):207-219.
Zhang,L.,Lin,D.,Zhang,Y.,Ma,G.,and Zhang,W.,2008.Ahomologue of sox11 predominantly expressed in the ovary of the orange-spotted grouper Epinephelus coioides.Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology,149(2):345-353.
Zhou,Q.,Shao,M.,Qin,Z.,Kyoung,H.K.,and Zhang,Z.,2010.Cloning,characterization,and expression analysis of the DEAD-box family genes,Fc-vasa and Fc-PL10a,in Chinese shrimp(Fenneropenaeus chinensis).Chinese Journal of Oceanology and Limnology,28(1):37-45.