Mapping of DNA Sex-Specific Markers and Genes Related to Sex Differentiation in Turbot (Scophthalmus maximus)

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• 作者：Ana Vi?as (1) anamaria.vinas@usc.es
  Xoana Taboada (1)
  Luis Vale (1)
  Diego Robledo (1)
  Miguel Hermida (2)
  Manel Vera (2)
  Paulino Martínez (2)
• 关键词：Turbot – Linkage map – Sex – Growth – Candidate genes – QTL
• 刊名：Marine Biotechnology
• 出版年：2012
• 出版时间：October 2012
• 年：2012
• 卷：14
• 期：5
• 页码：655-663
• 全文大小：224.5 KB
• 参考文献：1. Alfaqih MA, Brunelli JP, Drew RE, Thorgaard GH (2009) Mapping of five candidate sex-determining loci in rainbow trout (Oncorhynchus mykiss). BMC Genet 10:2
  2. Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 295:316–318
  3. Bagheri-Fam S, Sinclair AH, Koopman P, Harley VR (2009) Conserved regulatory modules in the Sox9 testis-specific enhancer predict roles for SOX, TCF/LEF, Forkhead, DMRT, and GATA proteins in vertebrate sex determination. Int J Biochem Cell Biol 42:472–477
  4. Batargias C, Dermitzakis E, Magoulas A, Zouros E (1998) Characterization of six polymorphic microsatellite markers in gilthead seabream, Sparus aurata. Mol Ecol 8:897–899
  5. Baynes SM, Verner-Jeffreys D, Howell BR (2006) Research on finfish cultivation. Sci Ser Tech Rep 32:1–64
  6. B?hne A, Schultheis C, Galiana-Arnoux D, Froschauer A, Zhou Q, Schmidt C, Selz Y, Ozouf-Costaz C, Dettai A, Segurens B, Couloux A, Bernard-Samain S, Barbe V, Chilmonczyk S, Brunet F, Darras A, Tomaszkiewicz M, Semon M, Schartl M, Volff JN (2009) Molecular analysis of the sex chromosomes of the platyfish Xiphophorus maculatus: towards the identification of a new type of master sexual regulator in vertebrates. Integr Zool 4:277–284
  7. Bouza C, Sánchez L, Martínez P (1994) Karyotypic characterization of turbot (Scophthalmus maximus) with conventional fluorochrome and restriction endonuclease-banding techniques. Mar Biol 120:609–613
  8. Bouza C, Hermida M, Pardo BG, Fernández C, Fortes GG, Castro J, Sánchez L, Presa P, Pérez M, Sanjuán A, de Carlos A, álvarez-Dios JA, Ezcurra S, Cal RM, Piferrer F, Martínez P (2007) A microsatellite genetic map of the turbot (Scophthalmus maximus). Genetics 177:2457–2467
  9. Bouza C, Hermida M, Millán A, Vilas R, Vera M, Fernández C, Calaza M, Pardo BG, Martínez P (2008) Characterization of EST-derived microsatellites for gene mapping and evolutionary genomics in turbot. Anim Genet 39:666–670
  10. Cal RM, Vidal S, Martínez P, álvarez-Blázquez B, Gómez C (2006) Survival, growth, gonadal development, and sex ratios of gynogenetic diploid turbot. J Fish Biol 68:401–413
  11. Casas L, Sánchez L, Orbán L (2011) Sex-associated DNA markers from turbot. Mar Biol Res 7:378–387
  12. Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, Van De Kant HJ, Wegner M, De Rooij DG, Behringer RR, Schedl A (2004) Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131:1891–1901
  13. Charlesworth B, Charlesworth D (1997) Rapid fixation of deleterious alleles by Muller’s ratchet. Genet Res 70:63–73
  14. Cnaani A, Levavi-Sivan B (2009) Sexual development in fish, practical applications for aquaculture. Sex Dev 3:164–175
  15. Cu?ado N, Terrones J, Sánchez L, Martínez P, Santos JL (2001) Synaptonemal complex analysis in spermatocytes and oocytes of turbot, Scophthalmus maximus (Pisces: Scophthalmidae). Genome 44:1143–1147
  16. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological and environmental influences. Aquaculture 208:191–364
  17. Diotel N, Page YL, Mouriec K, Tong SK, Pellegrini E, Vaillant C, Anglade I, Brion F, Pakdel F, Chung BC, Kah O (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 31:172–192
  18. Eshel O, Shirak A, Weller JI, Hulata G, Ron M (2012) Linkage and physical mapping of sex region on LG23 of Nile tilapia (Oreochromis niloticus). G3 (Bethesda) 2:35–42
  19. Foster JW, Graves JA (1994) An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc Natl Acad Sci U S A 91:1927–1931
  20. Graham P, Penn JKM, Schedl P (2002) Masters change, slaves remain. Bioessays 25:1–4
  21. Graves JAM (1998) Interactions between SRY and SOX genes in mammalian sex determination. Bioessays 20:264–269
  22. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a new family of embryonically expressed genes. Nature 346:245–250
  23. Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352–366
  24. Haffray P, Lebège E, Jeu S, Guennoc M, Guiguen Y, Baroiller JF, Fostier A (2009) Genetic determination and temperature effects on turbot Scophthalmus maximus sex differentiation: an investigation using steroid sex-inverted males and females. Aquaculture 294:30–36
  25. Hagiwara N (2011) Sox6, jack of all trades: a versatile regulatory protein in vertebrate development. Dev Dyn 240:1311–1321
  26. Hett AK, Ludwig A (2005) SRY-related (Sox) genes in the genome of European Atlantic sturgeon (Acipenser sturio). Genome 48:181–186
  27. Ijiri S, Kazeto V, Lokman PM, Adachi S, Yamauchi K (2003) Characterization of a cDNA encoding P-450 aromatase (CYP19) from Japanese eel ovary and its expression in ovarian follicles during induced ovarian development. Gen Comp Endocrinol 130:193–203
  28. Imsland A, Folkvord A, Stefansson O, Taranger L (1997) Sexual dimorphism in growth and maturation of turbot, Scophthalmus maximus (Rafinesque, 1810). Aquac Res 28:101–114
  29. Koopman P, Scheper G, Brenner S, Venkatesh B (2004) Origin and diversity of the Sox transcription factor gene family: genome-wide analysis in Fugu rubripes. Gene 328:177–186
  30. Lefebvre V (2010) The SoxD transcription factors-Sox5, Sox6, and Sox13-are key cell fate modulators. Int J Biochem Cell Biol 42:429–432
  31. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B (2007) Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 39:2195–2214
  32. Liu L, Zhou R (2001) Isolation of Sox11a, Sox11b and Sox19 genes from rice field eel (Monopterus albus) using degenerate primers and nested PCR. Aquat Sci 63:191–195
  33. Loukovitis D, Sarropoulou E, Tsigenopoulos CS, Batargias C, Magoulas A, Apostolidis AP, Chatziplis D, Kotoulas G (2011) Quantitative trait loci involved in sex determination and body growth in the gilthead sea bream (Spaurus aurata L.) through targeted genome scan. PLoS One 6:e16599
  34. Mank JE, Avise JC (2009) Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60–67
  35. Martínez P, Bouza C, Hermida M, Fernández J, Toro MA, Vera M, Pardo B, Millán A, Fernández C, Vilas R, Vi?as A, Sánchez L, Felip A, Piferrer F, Ferreiro I, Cabaleiro S (2009) Identification of the major sex-determining region of turbot (Scophthalmus maximus). Genetics 183:1443–1452
  36. 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 30:559–563
  37. McCormick MI, Ryen CA, Munday PL, Walker SPW (2010) Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish. PLoS One 5:e10616
  38. Moghadam HK, Poissant J, Fotherb H, Haidle L, Ferguson MM, Danzmann RG (2007) Quantitative trait loci for body weight, condition factor and age at sexual maturation in Arctic charr (Salvelinus alpinus): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Mol Genet Genomics 277:647–661
  39. Munakata A, Kobayashi M (2010) Endocrine control of sexual behavior in teleost fish. Gen Comp Endocrinol 165:456–468
  40. Navarro-Martín L, Galay-Burgos M, Sweeney G, Piferrer F (2009) Different sox17 transcripts during sex differentiation in sea bass, Dicentrarchus labrax. Mol Cell Endocrinol 299:240–251
  41. Okuda Y, Yoda H, Uchikawa M, Furutani-Seiki M, Takeda H, Kondoh H, Kamachi Y (2006) Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev Dyn 235:811–825
  42. Oshima Y, Naruse K, Nakamura Y, Nakamura M (2009) Sox3: a transcription factor for Cyp19 expression in the frog Rana rugosa. Gene 445:38–48
  43. Pala I, Klüver N, Thorsteinsdóttir S, Schartl M, Coelho MM (2008) Expression pattern of anti-Müllerian hormone (amh) in the hybrid fish complex of Squalius alburnoides. Gene 410:249–258
  44. Pardo BG, Fernández C, Millán A, Bouza C, Vázquez-López A, Vera M, Alvarez-Dios JA, Calaza M, Gómez-Tato A, Vázquez M, Cabaleiro S, Magari?os B, Lemos ML, Leiro JM, Martínez P (2008) Expressed sequence tags (ESTs) from immune tissues of turbot (Scophthalmus maximus) challenged with pathogens. BMC Vet Res 4:37
  45. Penman DJ, Piferrer F (2008) Fish gonadogenesis. Part I. Genetic and environmental mechanisms of sex determination. Rev Fish Sci 16(S1):14–32
  46. Piferrer F, Felip A, Blazquez M (1995) Control genético y fisiológico de las proporciones de sexos de los teleósteos y su aplicación en acuicultura. In: Aulas del Mar, Acuicultura, Biología Marina. Zamora S., Agulleiro y Garcia O. (eds) Murcia. pp: 75–109
  47. Piferrer F, Cal FRM, Gómez C, álvarez-Blázquez B, Castro J, Martínez P (2004) Induction of gynogenesis in the turbot (Scophthalmus maximus): effects of UV irradiation on sperm motility, the Hertwig effect and viability during the first 6 months of age. Aquaculture 238:403–419
  48. Poonlaphdecha S, Pepey E, Huang SH, Canonne M, Soler L, Mortaji S, Morand S, Pfennig F, Melard C, Baroiller JF (2011) Elevated amh gene expression in the brain of male tilapia (Oreochromis niloticus) during testis differentiation. Sex Dev 5:33–47
  49. Purdom CE, Thacker G (1980) Hybrid fish could have farm potential. Fish Farmer 3:34–35
  50. Rey R, Lukas-Croisier C, Lasala C, Bedecarras P (2003) AMH/MIS: what we know already about the gene, the protein and its regulation. Mol Cell Endocrinol 211:21–31
  51. Ruan X, Wang W, Kong J, YuF HX (2010) Genetic linkage mapping of turbot (Scophthalmus maximus L) using microsatellite markers and its application in QTL analysis. Aquaculture 308:89–100
  52. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  53. Sánchez-Molano E, Cerna A, Toro MA, Bouza C, Hermida M, Pardo BG, Cabaleiro S, Fernández J, Martínez P (2011) Detection of growth-related QTL in turbot (Scophthalmus maximus). BMC Genomics 12:473
  54. Schartl M (2004) Sex chromosome evolution in non-mammalian vertebrates. Curr Opin Gen Dev 14:634–641
  55. Shin HS, An KW, Park MS, Jeong MH, Choi CY (2009) Quantitative mRNA expression of sox3 and DMRT1 during sex reversal, and expression profiles after GnRHa administration in black porgy, Acanthopagrus schlegeli. Comp Biochem Physiol 154B:150–156
  56. Shirak A, Seroussi E, Cnaani A, Howe AE, Domokhovsky R, Zilberman N (2006) Amh and Dmrta2 genes map to tilapia (Oreochromis spp.) linkage group 23 within quantitative trait locus regions for sex determination. Genetics 174:1573–1581
  57. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA binding motif. Nature 346:240–244
  58. Taboada X, Robledo D, Del Palacio L, Rodeiro A, Felip A, Martínez P, Vi?as A (2012) Comparative expression analysis in mature gonads, liver and brain of turbot (Scophthalmus maximus) by cDNA-AFLPs. Gene 492(1):250–261
  59. Takamatsu N, Kanda H, Tsuchiya I, Yamada S, Ito M, Kabeno S, Shiba T, Yamashita S (1995) A gene that is related to SRY and is expressed in the testes encodes a leucine zipper-containing protein. Mol Cell Biol 15:3759–3766
  60. Tzchori I, Degani G, Hurvitz A, Moav B (2004) Cloning and developmental expression of the cytochrome P450 aromatase gene (CYP19) in the European eel (Anguilla anguilla). Gen Comp Endocrinol 138:271–280
  61. Vera M, Alvarez-Dios JA, Millán A, Pardo BG, Bouza C, Hermida M, Fernández C, de la Herrán R, Molina-Luzón MJ, Martínez P (2011) Validation of single nucleotide polymorphism (SNP) markers from an immune Expressed Sequence Tag (EST) turbot, Scophthalmus maximus, database. Aquaculture 313:31–41
  62. Vizziano D, Baron D, Randuineau G, Mahe S, Cauty C, 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
  63. Vizziano-Cantonnet D, Anglade I, Pellegrini E, Gueguen MM, Fostier A, Guiguen Y, Kah O (2011) Sexual dimorphism in the brain aromatase expression and activity, and in the central expression of other steroidogenic enzymes during the period of sex differentiation in monosex rainbow trout populations. Gen Comp Endocrinol 170:346–355
  64. Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280–294
  65. Wang XG, Orban L (2007) Anti-Müllerian hormone and 11 β-hydroxilase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males. Dev Dyn 236:1329–1338
  66. Wang R, Cheng HH, Xia LX, Guo YQ, Huang X, Zhou RJ (2003) Molecular cloning and expression of Sox17 in gonads during sex reversal in the rice field eel, a teleost fish with a characteristic of natural sex transformation. Biochem Biophys Res Commun 303:452–457
  67. Wegner M (1999) From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 27:1409–1420
  68. Wilkins AS (1995) Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17:71–77
  69. Yamashita A, Suzuki S, Fujitani K, Kojima M, Kanda H, Ito M, Takamatsu N, Yamashita S, Shiba T (1998) cDNA cloning of a novel rainbow trout SRY-type HMG box protein, rtSox23 and its functional analysis. Gene 209:193–200
  70. Yao B, Zhou L, Wang Y, Xia W, Gui JF (2007) Differential expression and dynamic changes of SOX3 during gametogenesis and sex inversion in protogynous hermaphroditic fish. J Exp Zool 307A:207–219
  71. Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Abe S, 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
• 作者单位：1. Departamento de Genética, Facultad de Biología (CIBUS), Universidad de Santiago de Compostela, Rúa Lope Gómez de Marzoa, s/n 15782, Santiago de Compostela, Spain2. Departamento de Genética, Facultad de Veterinaria, Universidad de Santiago de Compostela, Campus de Lugo, Avda das Ciencias, s/n 27002, Lugo, Spain
• ISSN：1436-2236

文摘

Production of all-female populations in turbot can increase farmer’s benefits since sexual dimorphism in growth in this species is among the highest within marine fish, turbot females reaching commercial size 3–6 months earlier than males. Puberty in males occurs earlier than in females, which additionally slows their growth. Thus, elucidating the mechanisms of sex determination and gonad differentiation is a relevant goal for turbot production. A ZZ/ZW sex determination mechanism has been suggested for this species, and four sex-related quantitative trait loci (QTL) were detected, the major one located in linkage group (LG) 5 and the three minor ones in LG6, LG8, and LG21. In the present work, we carried out a linkage analysis for several sex-related markers: (1) three anonymous sex-associated RAPD and (2) several candidate genes related to sex determination and gonad differentiation in other species (Sox3, Sox6, Sox8, Sox9, Sox17, Sox19, Amh, Dmrta2, Cyp19a, Cyp19b). We focused our attention on their co-localization with the major and minor sex-related QTL trying to approach to the master sex-determining gene of this species. Previously described growth-related QTL were also considered since the association observed between growth and sex determination in fish. Amh, Dmrta2, and one RAPD were located in LG5, while Sox9 and Sox17 (LG21), Cyp19b (LG6), and a second RAPD (LG8) co-mapped with suggestive sex-related QTL, thus supporting further analyses on these genes to elucidate the genetic basis of this relevant trait for turbot farming.