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Gonadal Development and Fertility of Triploid Grass Puffer Takifugu niphobles Induced by Cold Shock Treatment

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Abstract

Tiger puffer Takifugu rubripes is one of the most valuable fish species in Japan; however, there has not been much progress in their selective breeding until recently despite their potential in aquaculture. Their long generation time and the large body size of their broodstock make breeding difficult. Recently, we made a surrogate broodstock, which produced gametes of different species in salmonids. Therefore, by using closely related recipients, which have small body sizes and short generation times, it is possible to accelerate breeding of the tiger puffer. Thus, we considered the grass puffer Takifugu niphobles, which has a short generation time and a small maturation size, as a potential recipient for gamete production of the tiger puffer. Furthermore, if sterile triploid individuals are used as recipients, the resulting surrogate broodstock would produce only donor-derived gametes. Therefore, we examined conditions for inducing triploidy by suppressing meiosis II to retain the second polar body in grass puffer. We found that cold shock treatment, which is 5°C for 30 min starting from 5 min after fertilization, is optimal to obtain high triploidization and hatching rates. Although the resulting triploid grass puffers produced small amounts of gametes in both sexes, the offspring derived from the gametes could not live for over 3 days. Furthermore, we found that triploid grass puffer showed normal plasma sex steroid levels compared with diploids. These are important characteristics of triploid grass puffer as surrogate recipients used for germ cell transplantation.

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References

  • Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, Gelpke MD, Roach J, Oh T, Ho IY, Wong M, Detter C, Verhoef F, Predki P, Tay A, Lucas S, Richardson P, Smith SF, Clark MS, Edwards YJ, Doggett N, Zharkikh A, Tavtigian SV, Pruss D, Barnstead M, Evans C, Baden H, Powell J, Glusman G, Rowen L, Hood L, Tan YH, Elgar G, Hawkins T, Venkatesh B, Rokhsar D, Brenner S (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310

    Article  PubMed  CAS  Google Scholar 

  • Arakawa T, Takaya M, Inoue K, Takami I, Yamashita K (1987) An examination of the condition for triploid induction by cold shock in red and black sea breams. Bull Nagasaki Pref Inst Fish 13:25–30

    Google Scholar 

  • Brenner S, Elgar G, Sandford R, Macrae A, Venkatesh B, Aparicio S (1993) Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature 366:265–268

    Article  PubMed  CAS  Google Scholar 

  • Carrasco LAP, Doroshov S, Penman DJ, Bromage N (1998) Long-term, quantitative analysis of gametogenesis in autotriploid rainbow trout, Oncorhynchus mykiss. J Reprod Fertil 113:197–210

    Article  PubMed  CAS  Google Scholar 

  • Chuda H, Matsuyama M, Ikeda Y, Matsuura S (1997) Development of the maturation- and ovulation-induction method in cultured tiger puffer Takifugu rubripes by hormonal treatments. Nippon Suisan Gakkaishi 63:728–733

    Article  Google Scholar 

  • Ciruna B, Weidinger G, Knaut H, Thisse B, Thisse C, Raz E, Schier AF (2002) Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc Natl Acad Sci U S A 99:14919–14924

    Article  PubMed  CAS  Google Scholar 

  • Feindel NJ, Benfey TJ, Trippel EA (2010) Competitive spawning success and fertility of triploid male Atlantic cod Gadus morhua. Aquacult Environ Interact 1:47–55

    Article  Google Scholar 

  • Felip A, Zanny S, Carrillo M, Martinez G, Ramos J, Piferrer F (1997) Optimal conditions for the induction of triploidy in the sea bass (Dicentrarchus labrax L.). Aquaculture 152:287–298

    Article  Google Scholar 

  • Felip A, Piferrer F, Carrillo M, Zanuy S (2001a) Comparison of the gonadal development and plasma levels of sex steroid hormones in diploid and triploid sea bass, Dicentrarchus labrax L. J Exp Zool 290:384–395

    Article  PubMed  CAS  Google Scholar 

  • Felip A, Zanuy S, Carrillo M, Piferrer F (2001b) Induction of triploidy and gynogenesis in teleost fish with emphasis on marine species. Genetica 111:175–195

    Article  PubMed  CAS  Google Scholar 

  • Higuchi K, Takeuchi Y, Miwa M, Yamamoto Y, Tsunemoto K, Yoshizaki G (2011) Colonization, proliferation, and survival of intraperitoneally transplanted yellowtail Seriola quinqueradiata spermatogonia in nibe croaker Nibea mitsukurii recipient. Fish Sci 77:69–77

    Article  CAS  Google Scholar 

  • Hosoya S, Kaneko T, Suzuki Y, Hino A (2008) Individual variations in behavior and free cortisol responses to acute stress in tiger pufferfish Takifugu rubripes. Fish Sci 74:755–763

    Article  CAS  Google Scholar 

  • Kakimoto Y, Aida S, Arai K, Suzuki R (1994) Neuters occurred in methyltestosterone treated ocellated puffer Takifugu rubripes. Fish Genet Breed Sci 20:63–66

    Google Scholar 

  • Kawamura K, Ueda T, Aoki K, Hosoya K (1999) Spermatozoa in triploids of the rosy bitterling Rhodeus ocellatus ocellatus. J Fish Biol 55:420–432

    Article  Google Scholar 

  • Kikuchi K, Kai W, Hosokawa A, Mizuno N, Suetake H, Asahina K, Suzuki Y (2007) The sex-determining locus in the tiger pufferfish, Takifugu rubripes. Genetics 175:2039–2042

    Article  PubMed  CAS  Google Scholar 

  • Koedprang W, Na-Nakorn U (2000) Preliminary study on performance of triploid Thai silver barb, Puntius gonionotus. Aquaculture 190:211–221

    Article  Google Scholar 

  • Matsuyama M, Chuda H, Ikeda Y, Tanaka H, Matsuura S (1997) Induction of ovarian maturation and ovulation in cultured tiger puffer Takifugu rubripes by different hormonal treatments. Suisanzoshoku 40:67–73

    Google Scholar 

  • Maxime V (2008) The physiology of triploid fish: current knowledge and comparisons with diploid fish. Fish Fish 9:67–78

    Article  Google Scholar 

  • Miura T, Miura C, Ohta T, Nader MR, Todo T, Yamauchi K (1999) Estradiol-17β stimulates the renewal of spermatogonial stem cells in males. Biochem Biophys Res Commun 264:230–234

    Article  PubMed  CAS  Google Scholar 

  • Miyaki K (1992) Biological study of hybrid pufferfishes of the genus Takifugu, Tetraodontidae. Ph.D. thesis, Nagasaki University, Nagasaki

  • Miyaki K, Chuda H, Watanabe T, Mizuta K, Tsukasima Y, Yoshida N, Tabeta O (1998) Treatment of tiger puffer, Takifugu rubripes, eggs with tannic acid to eliminate their adhesiveness for seed production. Suisanzoshoku 46:97–100

    Google Scholar 

  • Miyaki K, Tabeta O, Kayano H (1995) Karyotypes in six species of pufferfishes genus Takifugu (Tetraodontidae, Tetraodontiformes). Fish Sci 61:594–598

    CAS  Google Scholar 

  • Miyaki K, Tachihara K, Ebisu R, Tsukashima Y, Matsumura Y, Fujita S, Hayashida G, Tabeta O (1992) Induction of ovarian maturation of the tiger puffer, Takifugu rubripes by gonadotropic hormone injections. Suisanzoshoku 40:439–442

    CAS  Google Scholar 

  • Mogami Y, Miyaki K, Arakawa T (1991) Spermatozoa of triploid Japanese parrotfish, Oplegnathus fascsiatus. Bull Nagasaki Pref Inst Fish 17:47–49

    Google Scholar 

  • Mol K, Byamungu N, Cuisset B, Yaron Z, Ofir M, Mèlard C, Castelli M, Kuhn ER (1994) Hormonal profile of growing male and female diploids and triploids of the blue tilapia, Oreochromis aureus, reared in intensive culture. Fish Physiol Biochem 13:209–218

    Article  CAS  Google Scholar 

  • Murata O (1998) Studies on the breeding of cultivated marine fishes. Bull Fish Lab Kinki Univ 6:49–56

    Google Scholar 

  • Nakamura M, Tsuchiya F, Iwahashi M, Nagahama Y (1993) Reproductive characteristics of precociously mature triploid male masu salmon, Oncorhynchus masou. Zool Sci 10:117–125

    Google Scholar 

  • Ojima Y, Kurishita A (1980) A new method to increase the number of mitotic cells in the kidney tissue for fish chromosome studies. Proc Jpn Acad 56:610–615

    Article  Google Scholar 

  • Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G (2006) Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc Natl Acad Sci U S A 103:2725–2729

    Article  PubMed  CAS  Google Scholar 

  • Okutsu T, Shikina S, Kanno M, Takeuchi Y, Yoshizaki G (2007) Production of trout offspring from triploid salmon parents. Science 317:1517

    Article  PubMed  CAS  Google Scholar 

  • Okutsu T, Kobayashi T, Takeuchi Y, Yoshizaki G (2008a) Identification of donor-derived germ cells and spermatozoa in xenogeneic recipient using species-specific primers against vasa gene in germ cell transplantation experiments. Fish Genet Breed 37:29–36

    Google Scholar 

  • Okutsu T, Takeuchi Y, Yoshizaki G (2008b) Spermatogonial transplantation in fish: production of trout offspring from salmon parents. Fisheries for Global Welfare and Environment. TERRAPUB, Tokyo, pp 209–219

    Google Scholar 

  • Piferrer F, Cal RM, Àlvarez-Blàzquez B, Sànchez L, Martìnez P (2000) Induction of triploidy in the turbot (Scophthalmus maximus). I. Ploidy determination and the effects of cold shocks. Aquaculture 188:79–90

    Article  Google Scholar 

  • Piferrer F, Beaumont A, Falguiere JC, Flajshans M, Haffray P, Colombo L (2009) Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 293:125–156

    Article  Google Scholar 

  • Purdom CE (1972) Induced polyploidy in plaice (Pleuronectes platessa) and its hybrid with the flounder (Platichthys flesus). Heredity 29:11–24

    Article  PubMed  CAS  Google Scholar 

  • Rashid H, Kitano H, Lee KH, Nii S, Shigematsu T, Kadomura K, Yamaguchi A, Matsuyama M (2007) Fugu (Takifugu rubripes) sexual differentiation: CYP19 regulation and aromatase inhibitor induced testicular development. Sex Dev 1:311–322

    Article  PubMed  CAS  Google Scholar 

  • Sugama K, Taniguchi N, Seki S, Nabeshima H (1992) Survival, growth and gonadal development of triploid red sea bream, Pagrus major (Temminck Schlegel): use of allozyme markers for ploidy and family identification. Aquac Res 23:149–159

    Article  Google Scholar 

  • Suzuki R (1963) Hybridization experiments in cyprinid fishes. IV. Reciprocal crosses between Biwia zezera and Gnathopogon elongatus elongatus. Bull Jpn Soc Sci Fish 29:655–657

    Article  Google Scholar 

  • Tabata K, Gorie S, Kawamura Y (1989) Growth, survival and maturation in the induced triploid hirame Paralichthys olivaceus. Suisanzoshoku 36:267–276

    Google Scholar 

  • Takeuchi Y, Yoshizaki G, Takeuchi T (2004) Surrogate broodstock produces salmonids. Nature 430:629–630

    Article  PubMed  CAS  Google Scholar 

  • Tiwary BK, Kirubagaran R, Ray AK (2000) Gonadal development in triploid Heteropneustes fossilis. J Fish Biol 57:1343–1348

    Article  Google Scholar 

  • Tiwary BK, Kirubagaran R, Ray AK (2004) The biology of triploid fish. Rev Fish Biol Fish 14:391–402

    Article  Google Scholar 

  • Ueno K (1985) Sterility and secondary sexual character of triploid Gnathopogon elongatus caerulescens. Fish Genet Breed Sci 10:37–41

    Google Scholar 

  • Uno Y (1955) Spawning habit and early development of a puffer, Fugu (Torafugu) niphobles (Jordan et Snyder). J Tokyo Univ Fish 41:169–183

    Google Scholar 

  • Weidinger G, Stebler J, Slanchev K, Dumstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E (2003) dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429–1434

    Article  PubMed  CAS  Google Scholar 

  • Wills PS, Sheehan RJ, Allen SK Jr (2000) Reduced reproductive capacity in diploid and triploid hybrid sunfish. Trans Am Fish Soc 129:30–40

    Article  Google Scholar 

  • Wong TT, Saito T, Crodian J, Collodi P (2011) Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae. Biol Reprod 84:1190–1197

    Article  PubMed  CAS  Google Scholar 

  • Yamaha E, Murakami M, Hada K, Otani S, Fujimoto T, Tanaka M, Sakao S, Kimura S, Sato S, Arai K (2003) Recovery of fertility in male hybrids of a cross between goldfish and common carp by transplantation of PGC (primordial germ cell)-containing graft. Genetica 119:121–131

    Article  PubMed  CAS  Google Scholar 

  • Yoshizaki G, Fujinuma K, Iwasaki Y, Okutsu T, Shikina S, Yazawa R, Takeuchi Y (2011) Spermatogonial transplantation in fish: a novel method for the preservation of genetic resources. Comp Biochem Physiol D Genomics Proteomics 6:55–61

    Article  Google Scholar 

  • Yoshizaki G, Okutsu T, Ichikawa M, Hayashi M, Takeuchi Y (2010) Sexual plasticity of rainbow trout germ cells. Anim Reprod 7:187–196

    Google Scholar 

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Acknowledgments

We thank Dr. K. Kikuchi, Fisheries Laboratory, The University of Tokyo, for discussion and support during the study. We also appreciate all the technical support from the members of the Nagasaki Prefectural Institute of Fisheries.

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Authors and Affiliations

  1. Nagasaki Prefectural Institute of Fisheries, 1551-4 Taira, Nagasaki-shi, Nagasaki, 851-2213, Japan

    Masaomi Hamasaki & Kadoo Miyaki

  2. Research Center for Advanced Science and Technology, Tokyo University of Marine Science and Technology, Banda 670, Tateyama-shi, Chiba, 294-0308, Japan

    Yutaka Takeuchi

  3. Department of Marine Biosciences, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477, Japan

    Goro Yoshizaki

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  1. Masaomi Hamasaki
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  2. Yutaka Takeuchi
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  4. Goro Yoshizaki
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Correspondence to Masaomi Hamasaki.

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Hamasaki, M., Takeuchi, Y., Miyaki, K. et al. Gonadal Development and Fertility of Triploid Grass Puffer Takifugu niphobles Induced by Cold Shock Treatment. Mar Biotechnol 15, 133–144 (2013). https://doi.org/10.1007/s10126-012-9470-3

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