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Dechorionation of fertilized eggs and embryonic development in arctic rainbow smelt Osmerus eperlanus mordax

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Abstract

In order to establish the basement for developmental engineering in osmerid fishes, a dechorionation technique and developmental stages were described using rainbow smelt Osmerus eperlanus mordax. Eggs of rainbow smelt were fertilized with tap water. One minute after fertilization, dechorionation was performed by treatment with smelt’s Ringer solution: SRS (128 mM NaCl, 2.8 mM KCl, 2.7 mM CaCl2) containing 0.1 % trypsin and adjusted to pH 11.0 with 1 N NaOH. The chorion was digested completely within 5 h at 10 °C and the resulting denuded embryos developed normally under artificial culture conditions with SRS containing 1.6 % albumen before embryonic body formation, and then tap water. At the hatching stage, the average survival rate was 37.8 %. Embryos without the chorion were highly transparent and organogenesis was easily observed under a stereomicroscope. Embryos developed slowly to the embryonic body formation stage (66 hours postfertilization (hpf)) and hatching stage (22 day postfertilization (dpf)) at 10 °C. The embryonic development of rainbow smelt was similar to that of zebrafish Danio rerio and generally followed the basic developmental pattern of teleosts. These characteristics suggest that developmental engineering technology developed in model fishes can be applied to rainbow smelt.

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References

  1. Nelson JS (2006) Family OSMERIDAE (172)–smelts. In: Nelson JS (ed) Fishes of the World, 4th edn. WILEY-Blackwell, New Jersey, pp 194–196

    Google Scholar 

  2. Nii H, Makiguchi Y, Fuji M, Ueda H (2010) Upriver spawning migration of shishamo smelt Spirinchus lanceolatus assessed by radio telemetry. Nippon Suisan Gakkaishi 76:855–869 (in Japanese with English abstract) doi:10.2331/suisan.76.855

  3. Carscadden JE, Frank KT, Leggett WC (2001) Ecosystem changes and the effects on capelin (Mallotus villosus), a major forage species. Can J Fish Aquat Sci 58:73–85. doi:10.1139/f00-185

    Article  Google Scholar 

  4. Ohta H, Kusuda S, Kudo S (1995) Motility of testicular spermatozoa in the Shishamo smelt Spirinchus lanceolatus. Nippon Suisan Gakkaishi 61:7–12 (in Japanese with English abstract) doi:10.2331/suisan.61.7

  5. Yamaha E, Saito T, Goto-Kazeto R, Arai K (2007) Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. J Sea Res 58:8–22. doi:10.1016/j.seares.2007.02.003

    Article  CAS  Google Scholar 

  6. Okutsu T, Yano A, Nagasawa K, Shikina S, Kobayashi T, Takeuchi Y, Yoshizaki G (2006) Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J Reprod Dev 52:685–693. doi:10.1262/jrd.18096

    Article  PubMed  Google Scholar 

  7. Yasui GS, Fujimoto T, Sakao S, Yamaha E, Arai K (2011) Production of loach (Misgurnus anguillicaudatus) germ-line chimera using transplantation of primordial germ cells isolated from cryopreserved blastomeres. J Anim Sci 89:2380–2388. doi:10.2527/jas.2010-3633 (Epub 2011 Mar 11)

    Article  CAS  PubMed  Google Scholar 

  8. Saito T, Goto-Kazeto R, Fujimoto T, Kawakami Y, Arai K, Yamaha E (2010) Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int J Dev Biol 54:1481–1486. doi:10.1387/ijdb.103111ts

    PubMed  Google Scholar 

  9. Saito T, Goto-Kazeto R, Kawakami Y, Nomura K, Tanaka H, Adachi S, Arai K, Yamaha E (2011) The mechanism for primordial germ-cell migration is conserved between japanese eel and zebrafish. PLoS One 6:e24460. doi:10.1371/journal.pone.002446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Saito T, Psˇenicˇka M, Goto R, Adachi S, Inoue K, Arai K, Yamaha E (2014) The Origin and Migration of Primordial Germ Cells in Sturgeons. PLoS ONE 9:e86861. doi:10.1371/journal.pone.0086861

    Article  PubMed  PubMed Central  Google Scholar 

  11. Saito T, Goto-Kazeto R, Arai K, Yamaha E (2008) Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol Reprod 78:159–166. doi:10.1095/biolreprod.107.060038

    Article  CAS  PubMed  Google Scholar 

  12. Inokuchi K, Nakatani T, Takatsu T, Takahashi T (1997) Gonadal maturation of female rainbow smelt Osmerus eperlanus mordax in Funka bay, Hokkaido. Nippon Suisan Gakkaishi 63:50–55 (in Japanese with English abstract) doi:10.2331/suisan.63.50

  13. Yanagimachi R (1957) Studies of fertilization in Clupea pallasii-VI. Fertilization of the egg deprived of the membrane. Jpn. J. Ichthyol. 6:41–47 (in Japanese) doi:10.11369/jji1950.7.61

  14. Iwamatsu T (1983) A new technique for dechorionation and observation on the development of the naked eggs in Oryzias latipes. J Exp Zool 228:83–89. doi:10.1002/jez.1402280109

    Article  Google Scholar 

  15. Ogawa N, Ooi Y (1968) The chorion and hatching enzyme of medaka Oryzias latipes. Zool. Mag. 77:151–156 (in Japanese with English abstract)

    Google Scholar 

  16. Sakai YT (1964) Method for removal of chorion and fertilization of the naked eggs in Oryzias latipes. Embryologia 5:357–368. doi:10.1111/j.1440-169X.1961.tb00101.x

    Article  Google Scholar 

  17. Kanoh Y, Yamamoto TS (1957) Removal of the membrane of the dog salmon egg by means of proteolytic enzymes. Nippon Suisan Gakkaishi 23:166–172. doi:10.2331/suisan.23.166

    Article  Google Scholar 

  18. Kawakami Y, Goto-Kazeto R, Saito T, Fujimoto T, Higaki S, Takahashi Y, Arai K, Yamaha E (2010) Generation of germ-line chimera zebrafish using primordial germ cells isolated from cultured blastomeres and cryopreserved embryoids. Int J Dev Biol 54:1493–1501. doi:10.1387/ijdb.093059yk

    Article  PubMed  Google Scholar 

  19. Yamaha E, Usui K, Onozato H, Hamada K (1986) A method for dechorionation in goldfish Cayassius auratus. Nippon Suisan Gakkaishi 52(11):1929–1934. doi:10.2331/suisan.52.1929

    Article  Google Scholar 

  20. Ito Y, Sakai H, Kondo M, Yamamoto K, Takagi M (1999) Development of denuded eggs of common carp. Aquaculture Sci. 47(2):257–261 (in Japanese with English abstract) doi: 10.11233/aquaculturesci1953.47.257

  21. Tachihara K, Kawaguchi K (2003) Morphological development of eggs, larvae and juveniles of laboratory-reared Ryukyu-ayu Plecoglossus altivelis ryukyuensis Fish. Sci. 69:323–330. doi:10.1046/j.1444-2906.2003.00624.x

    CAS  Google Scholar 

  22. Yamada J (1963) The normal developmental stage of the pond smelt, Hypomesus olidus (pallas). Bull Fac Fish Hokkaido Univ 14:121–126

    Google Scholar 

  23. Hikita T (1958) On the development of long-finned smelt, Spirinchus lanceolatus (Hikita). Scientific Reports of the Hokkaido Fish Hatchery 13:39–49 (in Japanese)

    Google Scholar 

  24. Yanagawa H (1978) Embryonic development and fry of the Kyuriuo, Osmerus eperlanus mordax (Mitchill). Bull Fac Fish Hokkaido Univ 29:195–198

    Google Scholar 

  25. Mizuno S, Sasaki Y, Omoto N, Imada K (2004) Elimination of adhesiveness in the eggs of shishamo smelt Spirinchus lanceolatus using kaolin treatment to achieve high hatching rate in an environment with a high iron concentration. Aquaculture 242:713–726. doi:10.1016/j.aquaculture.2004.09.019

    Article  CAS  Google Scholar 

  26. Hyafil F, Babinet C, Jacob F (1981) Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26:447–454. doi:10.1016/0092-8674(81)90214-2

    Article  CAS  PubMed  Google Scholar 

  27. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310. doi:10.1002/aja.100203030

    Article  CAS  PubMed  Google Scholar 

  28. Thai HY, Chang M, Liu SC, Abe G, Ota KG (2013) Embryonic development of goldfish (Carassius auratus) a model for the study of evolutionary change in developmental mechanisms by artificial selection. Dev Dyn 242:1262–1283. doi:10.1002/dvdy.24022

    Article  Google Scholar 

  29. Fujimoto T, Kataoka T, Sakao S, Saito T, Etsuro Y, Arai K (2006) Developmental stage and germ cell lineage of the Loach (Misgurnus anguillicaudatus). Zool Sci 23:977–989. doi:10.2108/zsj.23.977

    Article  PubMed  Google Scholar 

  30. Willemse MTHM, Denucé JM (1973) Hatching glands in the teleosts, Brachydanio rerio, Danio Malabaricus, Moenkhausia Oligolepis and Barbus schuberti. Dev. Growth Differ 15:169–177. doi:10.1111/j.1440-169X.1973.00169.x

    Article  Google Scholar 

  31. Yanai T, Ouji M, Iga T (1956) Development of the Hatching Glands in the Teleost, Hypomesus olidus (Pallas). Annot Zool Jpn 29:202–206

    Google Scholar 

  32. Strecker R, Seiler TB, Hollert H, Braunbeck T (2010) Oxygen requirements of zebrafish (Danio rerio) embryos in embryo toxicity tests with environmental samples. Comp. Biochem. Physiol. Part C: Toxicol Pharmacol 153:318–327. doi:10.1016/j.cbpc.2010.12.002

    Google Scholar 

  33. Kanamori A, Naruse K, Mitani H, Shima A, Hori H (2003) Genomic organization of ZP domain containing egg envelope genes in medaka (Oryzias latipes). Gene 305:35–45. doi:10.1016/S0378-1119(02)01211-8

    Article  CAS  PubMed  Google Scholar 

  34. Papadopoulou P, Galanopoulos VK, Hamodrakas SJ (1996) Molecular and supramolecular architecture of the Salmo gairdneri proteinaceous eggshell during development. J Struct Biol 116:399–412. doi:10.1006/jsbi.1996.0057

    Article  CAS  PubMed  Google Scholar 

  35. Ha CR, Iuchi I (1997) Extraction and partial characterization of egg envelope (chorion) transglutaminase of rainbow trout, Oncorhynchus mykiss: properties for Efficient Chorion Hardening. Comp Biochem Physiol 118:293–301. doi:10.1016/S0305-0491(97)00064-3

    Article  Google Scholar 

  36. Yoshizaki G, Oshiro T, Takashima F (1991) Introduction of carp α-globin gene into rainbow trout. Nippon Suisan Gakkaishi 57:819–824. doi:10.2331/suisan.57.819

    Article  CAS  Google Scholar 

  37. Saito T, Fujimoto T, Maegawa S, Inoue K, Tanaka M, Arai K, Yamaha E (2006) Visualization of primordial germ cells in vivo using GFP- nos1 3′ UTR mRNA. Int J Dev Biol 50:691–700. doi:10.1387/ijdb.062143ts

    Article  CAS  PubMed  Google Scholar 

  38. Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Dev 121:605–618. doi:10.1016/j.mod.2004.03.012

    Article  CAS  PubMed  Google Scholar 

  39. Saito T, Arai K, Yamaha E (2004) The Embryonic Development of Shima-ukigori, Gymnogobius opperiens. Aquacult. Sci. 52:177–184. doi:10.11233/aquaculturesci1953.52.177

    Google Scholar 

  40. Kawakami T, Okouchi H, Aritaki M, Aoyama J, Tsukamoto K (2011) Embryonic development and morphology of eggs and newly hatched larvae of Pacific herring Clupea pallasii. Fish Sci 77:183–190. doi:10.1007/s12562-010-0317-4

    Article  CAS  Google Scholar 

  41. Fujimoto T, Kataoka T, Otani S, Saito T, Aita T, Yamaha E, Arai K (2004) Embryonic stages from cleavage to gastrula in the loach Misgurnus anguillicaudatus. Zool Sci 21:747–755. doi:10.2108/zsj.21.747

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Fujimoto for assistance with this manuscript and to Dr. Shirakawa for statistical analysis. We also thank members of the Nanae Fresh-Water Station for assistance with obtaining experimental fish, conducting the experiments, and discussing the results. This study was supported by grants from the Bio-oriented Technology Research Advancement Institution (BRAIN) of Japan.

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Authors and Affiliations

  1. Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University, Nanae, Kameda, Hokkaido, 041-1105, Japan

    Eisuke Takahashi, Yutaka Kawakami & Etsuro Yamaha

  2. Laboratory of Aquaculture Genetics and Genomics, Faculty and Graduate School of Fisheries Science, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Eisuke Takahashi & Katsutoshi Arai

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  1. Eisuke Takahashi
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  4. Etsuro Yamaha
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Correspondence to Eisuke Takahashi.

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Takahashi, E., Kawakami, Y., Arai, K. et al. Dechorionation of fertilized eggs and embryonic development in arctic rainbow smelt Osmerus eperlanus mordax . Fish Sci 82, 639–652 (2016). https://doi.org/10.1007/s12562-016-0995-7

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  • DOI: https://doi.org/10.1007/s12562-016-0995-7

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