Chinese Science Bulletin

, Volume 58, Issue 1, pp 7–16 | Cite as

Progress in studies of fish reproductive development regulation

Open Access
Review Progress of Projects Supported by NSFC Hydrobiology


Mechanisms of the animal reproductive development are an important research field in life sciences. The study of the reproductive development and regulatory mechanisms in fishes is important for elucidating the mechanisms of animal reproduction. This paper summarizes recent advances in the mechanisms of fish sex determination and differentiation, of fish gonad development and maturation, and of fish germ cell development, as well as the according regulating strategies. Fishes comprise an evolutionary stage that links invertebrates and higher vertebrates. They include diversiform species, and almost all vertebrate types of reproduction have been found in fishes. All these will lead to important advances in the regulatory mechanisms of animal reproduction by using fishes as model organisms. It will also enable novel fish breeding techniques when new controllable on-off strategies of reproduction and/or sex in fishes have been developed.


fish reproduction regulation 


  1. 1.
    Gui J F, Zhu Z Y. Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull, 2012, 57: 1751–1760CrossRefGoogle Scholar
  2. 2.
    Gui J F, Zhou L. Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploidy Carassius auratus gibelio. Sci China Life Sci, 2010, 53: 409–415CrossRefGoogle Scholar
  3. 3.
    van Doom G S, Kirkpatrick M. Turnover of sex chromosomes induced by sexual conflict. Nature, 2007, 449: 909–912CrossRefGoogle Scholar
  4. 4.
    Ross J A, Urton J R, Boland J. Turnover of sex chromosomes in the stickleback fishes (gasterosteidae). PLoS Genet, 2009, 2: e1000391CrossRefGoogle Scholar
  5. 5.
    Arkhipchuk V V. Role of chromosomal and genome mutations in the evolution of bony fishes. Hydrobiol J, 1995, 31: 55–65Google Scholar
  6. 6.
    Traut W, Winking H. Meiotic chromosomes and stages of sex chromosome evolution in fish: Zebrafish, platyfish and guppy. Chromosome Res, 2001, 9: 659–672CrossRefGoogle Scholar
  7. 7.
    Artieri C G, Mitchell L A, Ng S H, et al. Identification of the sex-determining locus of Atlantic salmon (Salmo salar) on chromosome 2. Cytogenet Genome Res, 2006, 112: 152–159CrossRefGoogle Scholar
  8. 8.
    Zhao G, Yu Q X, Zhang W W, et al. The 5S rDNA related repetitive sequences in the sex chromosomes of the spiny eel (Mastacembelus aculeatus). Cytogenet Genome Res, 2008, 121: 143–148CrossRefGoogle Scholar
  9. 9.
    Lee B Y, Kocher T D. Exclusion of Wilms tumour (WT1b) and ovarian cytochrome P450 aromatase (CYP19A1) as candidates for sex determination genes in Nile tilapia (Oreochromis niloticus). Anim Genet, 2007, 38: 85–86CrossRefGoogle Scholar
  10. 10.
    von Hofsten J, Larsson A, Olsson P E. Novel steroidogenic factor-1 homolog (ff1d) is coexpressed with anti-Mullerian hormone (AMH) in zebrafish. Dev Dyn, 2005, 233: 595–604CrossRefGoogle Scholar
  11. 11.
    von Hofsten J, Olsson P E. Zebrafish sex determination and differentiation: Involvement of FTZ-F1 genes. Reprod Biol Endocrinol, 2005, 3: 63CrossRefGoogle Scholar
  12. 12.
    Nakamoto M, Wang D S, Suzuki A, et al. Dax1 suppresses P450arom expression in medaka ovarian follicles. Mol Reprod Dev, 2007, 74: 1239–1246CrossRefGoogle Scholar
  13. 13.
    Rogriguez-Mari A, Yan Y L, Bremiller R A, et al. Characterization and expression pattern of zebrafish Anti-Mullerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns, 2005, 5: 655–667CrossRefGoogle Scholar
  14. 14.
    Sawyer S J, Gerstner K A, Callard G V. Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: Gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen Comp Endocrinol, 2006, 147: 108–117CrossRefGoogle Scholar
  15. 15.
    Tang B, Hu W, Hao J, et al. Developmental expression of steroidogenic factor-1, cyp19a1a and cyp19a1b from common carp (Cyprinus carpio). Gen Comp Endocrinol, 2010, 167: 408–416CrossRefGoogle Scholar
  16. 16.
    Guiguen Y, Fostier A, Piferrer F, et al. Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol, 2010, 165: 352–366CrossRefGoogle Scholar
  17. 17.
    Wang D S, Kobayashi T, Zhou L Y. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol, 2007, 21: 712–725CrossRefGoogle Scholar
  18. 18.
    Vizziano D, Randuineau G, Baron D, et al. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn, 2007, 236: 2198–2206CrossRefGoogle Scholar
  19. 19.
    Cao M X, Duan J D, Cheng N N, et al. Sexually dimorphic and ontogenetic expression of dmrt1, cyp19a1a and cyp19a1b in Gobiocypris rarus. Comp Biochem Physiol A Mol Integr Physiol, 2012, 162: 303–309CrossRefGoogle Scholar
  20. 20.
    Matsuda M, Nagahama Y, Shinomiya A, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature, 2002, 417: 559–563CrossRefGoogle Scholar
  21. 21.
    Nanda I, Kondo M, Hornung U, et al. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA, 2002, 99: 11778–11783CrossRefGoogle Scholar
  22. 22.
    Hattori R S, Murai Y, Oura M, et al. A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA, 2012, 109: 2955–2959CrossRefGoogle Scholar
  23. 23.
    Li J, Phillips R B, Harwood A S, et al. Identification of the sex chromosomes of brown trout (Salmo trutta) and their comparison with the corresponding chromosomes in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). Cytogenet Genome Res, 2011, 133: 25–33CrossRefGoogle Scholar
  24. 24.
    Vandeputte M, Dupont-Nivet M, Chavanne H, et al. A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics, 2007, 176: 1049–1057CrossRefGoogle Scholar
  25. 25.
    Bradley K M, Breyer J P, Melville D B, et al. An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda), 2011, 1: 3–9Google Scholar
  26. 26.
    Liew W C, Bartfai R, Lim Z, et al. Polygenic sex determination system in zebrafish. PLoS One, 2012, 7: e34397CrossRefGoogle Scholar
  27. 27.
    Devlin R H, Nagahama Y. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture, 2002, 208: 191–364CrossRefGoogle Scholar
  28. 28.
    Conover D O, Kynard B E. Environmental sex determination: Interaction of temperature and genotype in a fish. Science, 1981, 213: 577–579CrossRefGoogle Scholar
  29. 29.
    Hayashi Y, Kobira H, Yamaguchi T, et al. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev, 2010, 77: 679–686CrossRefGoogle Scholar
  30. 30.
    Roemer U, Beisenherz W. Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). J Fish Biol, 1996, 48: 714–725Google Scholar
  31. 31.
    Conover D O, Daemond S B. Absence of temperature dependent sex determination in northern populations of two cyprinodontid fishes. Can J Zool, 1991, 69: 530–533CrossRefGoogle Scholar
  32. 32.
    Yamaguchi T, Yamaguchi S, Hirai T, et al. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder Paralichthys olivaceus. Biochem Biophys Res Commun, 2007, 359: 935–940CrossRefGoogle Scholar
  33. 33.
    Sehgal G K, Saxena P K. Effect of estrone on sex composition, growth and flesh composition in common carp, Cyprinus carpio communis (Linn.). J Aquacult Trop, 1997, 12: 289–295Google Scholar
  34. 34.
    Piferrer F, Baker I J, Donaldson E M. Effects of natural, synthetic, aromatizable, and nonaromatizable androgens in inducing male sex differentiation in genotypic female chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol, 1993, 91: 59–65CrossRefGoogle Scholar
  35. 35.
    Ito K, Mochida K, Fujii K. Molecular cloning of two estrogen receptors expressed in the testis of the Japanese common goby, Acanthogobius flavimanus. Zool Sci, 2007, 24: 986–996CrossRefGoogle Scholar
  36. 36.
    Chaves-Pozo E, Liarte S, Vargas-Chacoff L, et al. 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol Reprod, 2007, 76: 142–148CrossRefGoogle Scholar
  37. 37.
    Miura T, Higuchi M, Ozaki Y, et al. Progestin is an essential factor for the initiation of the meiosis in spermatogenetic cells of the eel. Proc Natl Acad Sci USA, 2006, 103: 7333–7338CrossRefGoogle Scholar
  38. 38.
    Liu X, Su H, Zhu P, et al. Molecular cloning, characterization and expression pattern of androgen receptor in Spinibarbus denticulatus. Gen Comp Endocrinol, 2009, 160: 93–101CrossRefGoogle Scholar
  39. 39.
    Quinitio G F, Caberoy N B, Reyes Jr D M. Induction of sex change in female Epinephelus coioides by social control. Isr J Aquacult, 1997, 49: 77–83Google Scholar
  40. 40.
    Bhandari R K, Komuro H, Nakamura S, et al. Gonadal restructuring and correlative steroid hormone profiles during natural sex change in protogynous honeycomb grouper (Epinephelus merra). Zool Sci, 2003, 20: 1399–1404CrossRefGoogle Scholar
  41. 41.
    Zhou L, Yao B, Xia W, et al. EST-based identification of genes expressed in the hypothalamus of male orange-spotted grouper (Epinephelus coioides). Aquaculture, 2006, 256: 129–139CrossRefGoogle Scholar
  42. 42.
    Alam M A, Kobayashi Y, Horiguchi R, et al. Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra. Gen Comp Endocrinol, 2008, 157: 75–85CrossRefGoogle Scholar
  43. 43.
    Huang X, Guo Y, Shui Y, et al. Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel. Biol Reprod, 2005, 73: 1017–1024CrossRefGoogle Scholar
  44. 44.
    Luo Y S, Hu W, Liu X C, et al. Molecular cloning and mRNA expression pattern of Sox9 during sex reversal in orange-spotted grouper (Epinephelus coioides). Aquaculture, 2010, 306: 322–328CrossRefGoogle Scholar
  45. 45.
    Kokokiris L, Fostier A, Athanassopoulou F, et al. Gonadal changes and blood sex steroids levels during natural sex inversion in the protogynous Mediterranean red porgy, Pagrus pagrus (Teleostei: Sparidae). Gen Comp Endocrinol, 2006, 149: 42–48CrossRefGoogle Scholar
  46. 46.
    Chang C F, Lee M F, Chen G L. Estradiol-17β associated with the sex reversal in protandrous black porgy, Acanthopagrus schlegeli. J Exp Zool, 1994, 268: 53–58CrossRefGoogle Scholar
  47. 47.
    Li G L, Liu X C, Lin H R. Effects of aromatizable and nonaromatizable androgens on the sex inversion of red-spotted grouper (Epinephelus akaara). Fish Physiol Biochem, 2006, 32: 25–33CrossRefGoogle Scholar
  48. 48.
    Kojima Y, Bhandari R K, Kobayashi Y, et al. Sex change of adult initial-phase male wrasse, Halichoeres trimaculatus by estradiol-17 beta treatment. Gen Comp Endocrinol, 2008, 156: 628–632CrossRefGoogle Scholar
  49. 49.
    Bhandari R K, Alam M A, Soyano K, et al. Induction of female-to-male sex change in the honeycomb grouper (Epinephelus merra) by 11-ketotestosterone treatments. Zool Sci, 2006, 23: 65–69CrossRefGoogle Scholar
  50. 50.
    Li G L, Liu X C, Lin H R. Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in redspotted grouper (Epinephelus akaara). Anim Reprod Sci, 2007, 99: 156–166CrossRefGoogle Scholar
  51. 51.
    Wu C J, Chen R D, Ye Y Z, et al. Production of all-female carp and its applications in fish cultivation. Aquaculture, 1990, 85: 327CrossRefGoogle Scholar
  52. 52.
    Liu H Q, Cui S Q, Hou C C, et al. YY supermale generated gynogenetically from XY female in Pelteobagrus fulvidraco (Richardson) (in Chinese). Acta Hydrobiol Sin, 2007, 31: 718–725Google Scholar
  53. 53.
    Liu Z, Wu F, Jiao B, et al. Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. J Endocrinol, 2007, 194: 223–241CrossRefGoogle Scholar
  54. 54.
    Wang D S, Zhou L Y, Kobayashi T, et al. Doublesex- and Mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology, 2010, 151: 1331–1340CrossRefGoogle Scholar
  55. 55.
    Rodriguez-Mari A, Canestro C, Bremiller R A, et al. Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet, 2010, 6: e1001034CrossRefGoogle Scholar
  56. 56.
    Slanchev K, Stebler J, de la Cueva-Mendez G, et al. Development without germ cells: The role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci USA, 2005, 102: 4074–4079CrossRefGoogle Scholar
  57. 57.
    Kurokawa H, Saito D, Nakamura S, et al. Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci USA, 2007, 104: 16958–16963CrossRefGoogle Scholar
  58. 58.
    Li W S, Lin H R. The endocrine regulation network of growth hormone synthesis and secretion in fish: Emphasis on the signal integration in somatotropes. Sci China Life Sci, 2010, 53: 462–470CrossRefGoogle Scholar
  59. 59.
    Hu W, Wang Y P, Zhu Z Y. Progress in the evaluation of transgenic fish for possible ecological risk and its containment strategies. Sci China Life Sci, 2007, 50: 573–579CrossRefGoogle Scholar
  60. 60.
    Hu W, Zhu Z Y. Integration mechanisms of transgenes and population fitness of GH transgenic fish. Sci China Life Sci, 2010, 53: 401–408CrossRefGoogle Scholar
  61. 61.
    Xu H Y, Li M Y, Gui J F, et al. Fish germ cells. Sci China Life Sci, 2010, 53: 435–446CrossRefGoogle Scholar
  62. 62.
    Olsen L C, Aasland R, Fjose A. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev, 1997, 66: 95–105CrossRefGoogle Scholar
  63. 63.
    Kawakami Y, Saito T, Fujimoto T, et al. Visualization and motility of primordial germ cells using green fluorescent protein fused to 3′UTR of common carp nanos-related gene. Aquaculture, 2011, 317: 245–250CrossRefGoogle Scholar
  64. 64.
    Raz E, Hopkins N. Primordial germ-cell development in zebrafish. Results Probl Cell Differ, 2002, 40: 166–179Google Scholar
  65. 65.
    Cao M X, Yang Y H, Xu H Y, et al. Germ cell specific expression of Vasa in rare minnow, Gobiocypris rarus. Comp Biochem Physiol A Mol Integr Physiol, 2012, 162: 163–170CrossRefGoogle Scholar
  66. 66.
    Shinomiya A, Tanaka M, Kobayashi T, et al. The vasa-like gene, olvas, identifies the migration path of primordial germ cells during embryonic body formation stage in the medaka, Oryzias latipes. Dev Growth Differ, 2000, 42: 317–326CrossRefGoogle Scholar
  67. 67.
    Blaser H, Eisenbeiss S, Neumann M, et al. Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J Cell Sci, 2005, 118: 4027–4038CrossRefGoogle Scholar
  68. 68.
    Raz E, Reichman-Fried M. Attraction rules: Germ cell migration in zebrafish. Curr Opin Genet Dev, 2006, 16: 355–359CrossRefGoogle Scholar
  69. 69.
    Boldajipour B, Mahabaleshwar H, Kardash E, et al. Control of chemokine-guided cell migration by ligand sequestration. Cell, 2008, 132: 463–473CrossRefGoogle Scholar
  70. 70.
    Herpin A, Fischer P, Liedtke D, et al. Sequential SDF1a and b-induced mobility guides medaka PGC migration. Dev Biol, 2008, 320: 319–327CrossRefGoogle Scholar
  71. 71.
    Kunwar P S, Siekhaus D E, Lehmann R. In vivo migration: A germ cell perspective. Annu Rev Cell Dev Biol, 2006, 22: 237–265CrossRefGoogle Scholar
  72. 72.
    Herpin A, Schindler D, Kraiss A, et al. Inhibition of primordial germ cell proliferation by the medaka male determining gene Dmrt1bY. BMC Dev Biol, 2007, 7: 99CrossRefGoogle Scholar
  73. 73.
    Shiraishi E, Yoshinaga N, Miura T, et al. Mullerian inhibiting substance is required for germ cell proliferation during early gonadal differentiation in medaka (Oryzias latipes). Endocrinology, 2008, 149: 1813–1819CrossRefGoogle Scholar
  74. 74.
    Houwing S, Kamminga L M, Berezikov E, et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell, 2007, 129: 69–82CrossRefGoogle Scholar
  75. 75.
    Schulz R W, de França L R, Lareyre J J, et al. Spermatogenesis in fish. Gen Comp Endocrinol, 2010, 165: 390–411CrossRefGoogle Scholar
  76. 76.
    Lubzens E, Young G, Bobe J, et al. Oogenesis in teleosts: How fish eggs are formed. Gen Comp Endocrinol, 2010, 165: 367–389CrossRefGoogle Scholar
  77. 77.
    Zohar Y, Munoz-Cueto J A, Elizur A, et al. Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol, 2010, 165: 438–455CrossRefGoogle Scholar
  78. 78.
    de Roux N, Genin E, Carel J C, et al. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA, 2003, 100: 10972–10976CrossRefGoogle Scholar
  79. 79.
    Tena-Sempere M, Felip A, Gomez A, et al. Comparative insights of the kisspeptin/kisspeptin receptor system: Lessons from non-mammalian vertebrates. Gen Comp Endocrinol, 2012, 175: 234–243CrossRefGoogle Scholar
  80. 80.
    Parhar I S, Ogawa S, Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology, 2004, 145: 3613–3618CrossRefGoogle Scholar
  81. 81.
    Kitahashi T, Ogawa S, Parhar I. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology, 2009, 150: 821–831CrossRefGoogle Scholar
  82. 82.
    Li S, Zhang Y, Liu Y, et al. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J Endocrinol, 2009, 201: 407–418CrossRefGoogle Scholar
  83. 83.
    Pasquier J, Lafont A G, Leprince J, et al. First evidence for a direct inhibitory effect of kisspeptins on LH expression in the eel, Anguilla anguilla. Gen Comp Endocrinol, 2011, 173: 216–225CrossRefGoogle Scholar
  84. 84.
    Tsutsui K, Bentley G E, Ubuka T, et al. The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen Comp Endocrinol, 2007, 153: 365–370CrossRefGoogle Scholar
  85. 85.
    Zhang Y, Li S, Liu Y, et al. Structural diversity of the gnih/gnih receptor system in teleost: Its involvement in early development and the negative control of LH release. Peptides, 2010, 31: 1034–1043CrossRefGoogle Scholar
  86. 86.
    Moussavi M, Wlasichuk M, Chang J P, et al. Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish. Mol Cell Endocrinol, 2012, 350: 53–60CrossRefGoogle Scholar
  87. 87.
    Trudeau V L. Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Rev Reprod, 1997, 2: 55–68CrossRefGoogle Scholar
  88. 88.
    Popesku J T, Martyniuk C J, Mennigen J, et al. The goldfish (Carassius auratus) as a model for neuroendocrine signaling. Mol Cell Endocrinol, 2008, 293: 43–56CrossRefGoogle Scholar
  89. 89.
    Xu J, Huang W, Zhong C R, et al. Defining global gene expression changes of the hypothalamic-pituitary-gonadal axis in female sGnRH-antisense transgenic common carp (Cyprinus carpio). PLoS One, 2011, 6: e21057CrossRefGoogle Scholar
  90. 90.
    Uzbekova S, Chyb J, Ferriere F, et al. Transgenic rainbow trout expressed sGnRH-antisense RNA under the control of sGnRH promoter of Atlantic salmon. J Mol Endocrinol, 2000, 25: 337–350CrossRefGoogle Scholar
  91. 91.
    Maclean N, Hwang G, Molina A, et al. Reversibly-sterile fish via transgenesis. ISB News Report, 2003, 1–3Google Scholar
  92. 92.
    Hu W, Li S F, Tang B, et al. Antisense for gonadotropin-releasing hormone reduces gonadotropin synthesis and gonadal development in transgenic common carp (Cyprinus carpio). Aquaculture, 2007, 271: 498–506CrossRefGoogle Scholar
  93. 93.
    Weidinger G., Stebler J, Slanchev K, et al. dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol, 2003, 13: 1429–1434CrossRefGoogle Scholar
  94. 94.
    Koprunner M, Thisse C, Thisse B, et al. A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev, 2001, 15: 2877–2885Google Scholar
  95. 95.
    Ramasamy S, Wang H, Quach H N, et al. Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. Dev Biol, 2006, 292: 393–406CrossRefGoogle Scholar
  96. 96.
    Hsu C C, Hou M F, Hong J R, et al. Inducible male infertility by targeted cell ablation in zebrafish testis. Mar Biotechnol, 2010, 12: 466–478CrossRefGoogle Scholar
  97. 97.
    Hu S Y, Lin P Y, Liao C H, et al. Nitroreductase-mediated gonadal dysgenesis for infertility control of genetically modified zebrafish. Mar Biotechnol, 2010, 12: 569–578CrossRefGoogle Scholar
  98. 98.
    Wakamatsu Y, Ju B, Pristyaznhyuk I, et al. Fertile and diploid nuclear transplants derived from embryonic cells of a small laboratory fish, medaka (Oryzias latipes). Proc Natl Acad Sci USA, 2001, 98: 1071–1076CrossRefGoogle Scholar
  99. 99.
    Hu W, Wang Y P, Chen S P, et al. Nuclear transplantation in different strains of zebrafish. Chin Sci Bull, 2002, 47: 1277–1280CrossRefGoogle Scholar
  100. 100.
    Lee K Y, Huang H, Ju B, et al. Cloned zebrafish by nuclear transfer from long-term-cultured cells. Nat Biotechnol, 2002, 20: 795–799Google Scholar
  101. 101.
    Liu T M, Liu L, Wei Q W, et al. Sperm nuclear transfer and transgenic production in the fish medaka. Int J Biol Sci, 2011, 7: 469–475CrossRefGoogle Scholar
  102. 102.
    Luo D J, Hu W, Chen S P, et al. Identification of differentially expressed genes between cloned and zygote-developing zebrafish (Danio rerio) embryos at the dome stage using suppression subtractive hybridization. Biol Reprod, 2009, 80: 674–684CrossRefGoogle Scholar
  103. 103.
    Luo D J, Hu W, Chen S P, et al. Critical developmental stages for the efficiency of somatic cell nuclear transfer in zebrafish. Int J Biol Sci, 2011, 7: 476–486CrossRefGoogle Scholar
  104. 104.
    Takeuchi Y, Yoshizaki G, Takeuchi T. Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biol Reprod, 2003, 69: 1142–1149CrossRefGoogle Scholar
  105. 105.
    Saito T, Goto-Kazeto R, Arai K, et al. Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol Reprod, 2008, 78: 159–166CrossRefGoogle Scholar
  106. 106.
    Saito T, Goto-Kazeto R, Fujimoto T, et al. Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int J Dev Biol, 2010, 54: 1481–1486Google Scholar
  107. 107.
    Nobrega R H, Greebe C D, van de Kant H, et al. Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PLoS One, 2010, 5: e12808CrossRefGoogle Scholar
  108. 108.
    Majhi S K, Hattori R S, Yokota M, et al. Germ cell transplantation using sexually competent fish: An approach for rapid propagation of endangered and valuable germlines. PLoS One, 2009, 4: e6132CrossRefGoogle Scholar
  109. 109.
    Okutsu T, Shikina S, Kanno M, et al. Production of trout offspring from triploid salmon parents. Science, 2007, 317: 1517CrossRefGoogle Scholar
  110. 110.
    Lacerda S M, Batlouni S R, Costa G M. A new and fast technique to generate offspring after germ cells transplantation in adult fish: The Nile tilapia (Oreochromis niloticus) model. PLoS One, 2010, 5: e10740CrossRefGoogle Scholar
  111. 111.
    Hong Y H, Winkler C, Schartl M. Pluripotency and differentiation of embryonic stem cell lines from the medakafish (Oryzias latipes). Mech Dev, 1996, 60: 33–44CrossRefGoogle Scholar
  112. 112.
    Yi M S, Hong N, Li Z D, et al. Medaka fish stem cells and their applications. Sci China Life Sci, 2010, 53: 426–434CrossRefGoogle Scholar
  113. 113.
    Chen S L, Sha Z X, Ye H Q, et al. Pluripotency and chimera competence of an embryonic stem cell line from the sea perch (Lateolabrax japonicus). Mar Biotechnol, 2007, 9: 82–91CrossRefGoogle Scholar
  114. 114.
    Fan L C, Collodi P. Zebrafish embryonic stem cells. Methods Enzymol, 2006, 418: 64–77CrossRefGoogle Scholar
  115. 115.
    Yi M S, Hong N, Hong Y H. Generation of medaka fish haploid embryonic stem cells. Science, 2009, 326: 430–433CrossRefGoogle Scholar
  116. 116.
    Hong Y H, Liu T M, Zhao H B, et al. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci USA, 2004, 101: 8011–8016CrossRefGoogle Scholar
  117. 117.
    Sakai N. In vitro male germ cell cultures of zebrafish. Methods, 2006, 39: 239–245CrossRefGoogle Scholar
  118. 118.
    Fan L C, Moon J, Wong T T, et al. Zebrafish primordial germ cell cultures derived from vasa: RFP transgenic embryos. Stem Cells Dev, 2008, 17: 585–597CrossRefGoogle Scholar
  119. 119.
    Shikina S, Yoshizaki G. Improved in vitro culture conditions to enhance the survival, mitotic activity, and transplantability of rainbow trout type A spermatogonia. Biol Reprod, 2010, 83: 268–276CrossRefGoogle Scholar
  120. 120.
    Panda R P, Barman H K, Mohapatra C. Isolation of enriched carp spermatogonial stem cells from Labeo rohita testis for in vitro propagation. Theriogenology, 2011, 76: 241–251CrossRefGoogle Scholar
  121. 121.
    Nakamura S, Kobayashi K, Nishimura T, et al. Identification of germline stem cells in the ovary of the teleost medaka. Science, 2010, 328: 1561–1563CrossRefGoogle Scholar

Copyright information

© The Author(s) 2012

Authors and Affiliations

  1. 1.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina

Personalised recommendations