Early embryonic development in pikeperch (Sander lucioperca) related to micromanipulation

https://doi.org/10.17221/35/2015-CJASCitation:Güralp H., Pocherniaieva K., Blecha M., Policar T., Pšenička M., Saito T. (2016): Early embryonic development in pikeperch (Sander lucioperca) related to micromanipulation. Czech J. Anim. Sci., 61: 273-280.
download PDF
Recently, transplantation of germ cells has attracted attention as a potential technique for efficient reproduction of fish. One of the well-proven techniques to deliver donor germ cells into a recipient is the transplantation of primordial germ cells (PGCs) during the blastula stage. Nevertheless, the application of such techniques so far has been limited to model fish species such as zebrafish, due to the lack of information about early development in many fish species. We propose that pikeperch (Sander lucioperca) can be a useful model species for establishing this technique in the order Perciformes, which includes commercially and ecologically important marine species. In this study, we described the important events, namely, embryonic staging, yolk syncytial layer (YSL) formation, and midblastula transition (MBT) during the blastula stage in pikeperch to obtain basic information about early embryonic development. The chorion was softened by treating with 0.2% trypsin and 0.4% urea in Ringer’s solution so as to remove it easily by forceps. Although the first cleavage occurred at about 2.5 h post fertilization, blastomeres divided approximately every one hour after this at 15°C. The YSL was formed after the breakdown of marginal cells during the 512- to 1k-cell stage. Cell division analysis by 4’-6-diaminido-2-phenylindole (DAPI) staining revealed that transition from synchronous to asynchronous division occurred after the 10th cleavage (1k-cell stage). Our results indicate that zygotic gene expression (MBT) starts after this stage. Next, we performed blastodisc isolation assay to find the competent stage for embryonic manipulation. Embryos were manipulated by using a microneedle every hour from the 512-cell to the sphere stage, and then developmental rates were evaluated at the hatching stage. The highest survival rate was obtained when we performed this manipulation at the 1k-cell stage. These results clearly showed that the MBT is the best stage for transplantation of PGCs or any cells in pikeperch.
References:
Chen S.R., Kimelman D. (2000): The role of the yolk syncytial layer in germ layer patterning in zebrafish. Development, 127, 4681–4689.
 
FAO (2015): Cultured Aquatic Species Information Programme: Sander lucioperca (Linnaeus, 1758). FAO Fisheries and Aquaculture Department. Available from www.fao.org/fishery/culturedspecies/Sander_lucioperca/en (accessed Oct 27, 2015).
 
Fujimoto Takafumi, Kataoka Takashi, Otani Satoshi, Saito Taiju, Aita Takanori, Yamaha Etsuro, Arai Katsutoshi (2004): Embryonic Stages from Cleavage to Gastrula in the Loach Misgurnus anguillicaudatus. Zoological Science, 21, 747-755  https://doi.org/10.2108/zsj.21.747
 
Ho R., Kimmel C. (1993): Commitment of cell fate in the early zebrafish embryo. Science, 261, 109-111  https://doi.org/10.1126/science.8316841
 
Kane D.A., Kimmel C.B. (1993): The zebrafish midblastula transition. Development, 119, 447–456.
 
Kimmel C.B., Law R.D. (1985): Cell lineage of zebrafish blastomeres: I. cleavage pattern and cytoplasmic bridges between cells. Developmental Biology, 108, 78–85.
 
Kimmel Charles B., Ballard William W., Kimmel Seth R., Ullmann Bonnie, Schilling Thomas F. (1995): Stages of embryonic development of the zebrafish. Developmental Dynamics, 203, 253-310  https://doi.org/10.1002/aja.1002030302
 
Křišt’an Jiří, Alavi Sayyed Mohammad Hadi, Stejskal Vlastimil, Policar Tomáš (2013): Hormonal induction of ovulation in pikeperch (Sander lucioperca L.) using human chorionic gonadotropin (hCG) and mammalian GnRH analogue. Aquaculture International, 21, 811-818  https://doi.org/10.1007/s10499-012-9572-y
 
Lacerda Samyra M. S. N., Batlouni Sergio R., Costa Guilherme M. J., Segatelli Tânia M., Quirino Bruno R., Queiroz Bruno M., Kalapothakis Evanguedes, França Luiz R., Wang Hongmei (2010): A New and Fast Technique to Generate Offspring after Germ Cells Transplantation in Adult Fish: The Nile Tilapia (Oreochromis niloticus) Model. PLoS ONE, 5, e10740-  https://doi.org/10.1371/journal.pone.0010740
 
Lin S., Long W., Chen J., Hopkins N. (1992): Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos.. Proceedings of the National Academy of Sciences, 89, 4519-4523  https://doi.org/10.1073/pnas.89.10.4519
 
Majhi Sullip K., Hattori Ricardo S., Yokota Masashi, Watanabe Seiichi, Strüssmann Carlos A., Orban Laszlo (2009): Germ Cell Transplantation Using Sexually Competent Fish: An Approach for Rapid Propagation of Endangered and Valuable Germlines. PLoS ONE, 4, e6132-  https://doi.org/10.1371/journal.pone.0006132
 
Mizuno Toshiro, Yamaha Etsuro, Wakahara Masami, Kuroiwa Atsushi, Takeda Hiroyuki (1996): Mesoderm induction in zebrafish. Nature, 383, 131-132  https://doi.org/10.1038/383131a0
 
Nakagawa Masahiro, Kobayashi Toru, Ueno Koichi (2002): Production of germline chimera in loach (Misgurnus anguillicaudatus) and proposal of new method for preservation of endangered fish species. Journal of Experimental Zoology, 293, 624-631  https://doi.org/10.1002/jez.10184
 
Newport John, Kirschner Marc (1982): A major developmental transition in early xenopus embryos: II. control of the onset of transcription. Cell, 30, 687-696  https://doi.org/10.1016/0092-8674(82)90273-2
 
Okutsu T., Shikina S., Kanno M., Takeuchi Y., Yoshizaki G. (): Production of Trout Offspring from Triploid Salmon Parents. Science, 317, 1517-1517  https://doi.org/10.1126/science.1145626
 
Oprea D., Marica N., Costache M. (2014): Research considering embryonic development of pikeperch (Sander lucioperca) under artificial-controlled spawning conditions. Journal of Animal Science and Biotechnology, 47, 229–234.
 
Saito Taiju, Goto-Kazeto Rie, Kawakami Yutaka, Nomura Kazuharu, Tanaka Hideki, Adachi Shinji, Arai Katsutoshi, Yamaha Etsuro, Klymkowsky Michael (2011): The Mechanism for Primordial Germ-Cell Migration Is Conserved between Japanese Eel and Zebrafish. PLoS ONE, 6, e24460-  https://doi.org/10.1371/journal.pone.0024460
 
Schlumberger O., Proteau J.-P. (1996): Reproduction of pike-perch (Stizostedion lucioperca) in captivity. Journal of Applied Ichthyology, 12, 149-152  https://doi.org/10.1111/j.1439-0426.1996.tb00080.x
 
Takeuchi Yutaka, Yoshizaki Goro, Takeuchi Toshio (2001): Production of germ-line chimeras in rainbow trout by blastomere transplantation. Molecular Reproduction and Development, 59, 380-389  https://doi.org/10.1002/mrd.1044
 
Tsai Hsin-Yuan, Chang Mariann, Liu Shih-Chieh, Abe Gembu, Ota Kinya G. (2013): Embryonic development of goldfish ( Carassius auratus ): A model for the study of evolutionary change in developmental mechanisms by artificial selection. Developmental Dynamics, 242, 1262-1283  https://doi.org/10.1002/dvdy.24022
 
Wakamatsu Y., Ozato K., Hashimoto H., Kinoshita M., Sakaguchi M., Iwamatsu T. (1993): Generation of germ-line chimeras in medaka (Oryzias latipes). Molecular Marine Biology and Biotechnology, 2, 325–332.
 
Yamaha Etsuro, Mizuno Toshiro, Hasebe Yutaka, Takeda Hiroyuki, Yamazaki Fumio (1998): Dorsal specification in blastoderm at the blastula stage in the goldfish, Carassius auratus. Development, Growth and Differentiation, 40, 267-275  https://doi.org/10.1046/j.1440-169X.1998.t01-1-00002.x
 
Yamaha Etsuro, Mizuno Toshiro, Matsushita Ken, Hasebe Yutaka (1999): Developmental Staging in Goldfish during the Pre-gastrula Stage.. NIPPON SUISAN GAKKAISHI, 65, 709-717  https://doi.org/10.2331/suisan.65.709
 
Yamaha E., Kazama-Wakabayashi M., Otani S., Fujimoto T., Arai K. (2001): Germ-line chimera by lower part blastoderm transplantation between diploid goldfish and triploid crucian carp. Genetica, 111, 227–236. https://doi.org/10.1023/A:1013780423986
 
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. https://doi.org/10.1023/A:1026061828744
 
Yamaha Etsuro, Saito Taiju, Goto-Kazeto Rie, Arai Katsutoshi (2007): Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. Journal of Sea Research, 58, 8-22  https://doi.org/10.1016/j.seares.2007.02.003
 
Yoon C., Kawakami K., Hopkins N. (1997): Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development, 124, 3157–3165.
 
Chen S.R., Kimelman D. (2000): The role of the yolk syncytial layer in germ layer patterning in zebrafish. Development, 127, 4681–4689.
 
FAO (2015): Cultured Aquatic Species Information Programme: Sander lucioperca (Linnaeus, 1758). FAO Fisheries and Aquaculture Department. Available from www.fao.org/fishery/culturedspecies/Sander_lucioperca/en (accessed Oct 27, 2015).
 
Fujimoto Takafumi, Kataoka Takashi, Otani Satoshi, Saito Taiju, Aita Takanori, Yamaha Etsuro, Arai Katsutoshi (2004): Embryonic Stages from Cleavage to Gastrula in the Loach Misgurnus anguillicaudatus. Zoological Science, 21, 747-755  https://doi.org/10.2108/zsj.21.747
 
Ho R., Kimmel C. (1993): Commitment of cell fate in the early zebrafish embryo. Science, 261, 109-111  https://doi.org/10.1126/science.8316841
 
Kane D.A., Kimmel C.B. (1993): The zebrafish midblastula transition. Development, 119, 447–456.
 
Kimmel C.B., Law R.D. (1985): Cell lineage of zebrafish blastomeres: I. cleavage pattern and cytoplasmic bridges between cells. Developmental Biology, 108, 78–85.
 
Kimmel Charles B., Ballard William W., Kimmel Seth R., Ullmann Bonnie, Schilling Thomas F. (1995): Stages of embryonic development of the zebrafish. Developmental Dynamics, 203, 253-310  https://doi.org/10.1002/aja.1002030302
 
Křišt’an Jiří, Alavi Sayyed Mohammad Hadi, Stejskal Vlastimil, Policar Tomáš (2013): Hormonal induction of ovulation in pikeperch (Sander lucioperca L.) using human chorionic gonadotropin (hCG) and mammalian GnRH analogue. Aquaculture International, 21, 811-818  https://doi.org/10.1007/s10499-012-9572-y
 
Lacerda Samyra M. S. N., Batlouni Sergio R., Costa Guilherme M. J., Segatelli Tânia M., Quirino Bruno R., Queiroz Bruno M., Kalapothakis Evanguedes, França Luiz R., Wang Hongmei (2010): A New and Fast Technique to Generate Offspring after Germ Cells Transplantation in Adult Fish: The Nile Tilapia (Oreochromis niloticus) Model. PLoS ONE, 5, e10740-  https://doi.org/10.1371/journal.pone.0010740
 
Lin S., Long W., Chen J., Hopkins N. (1992): Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos.. Proceedings of the National Academy of Sciences, 89, 4519-4523  https://doi.org/10.1073/pnas.89.10.4519
 
Majhi Sullip K., Hattori Ricardo S., Yokota Masashi, Watanabe Seiichi, Strüssmann Carlos A., Orban Laszlo (2009): Germ Cell Transplantation Using Sexually Competent Fish: An Approach for Rapid Propagation of Endangered and Valuable Germlines. PLoS ONE, 4, e6132-  https://doi.org/10.1371/journal.pone.0006132
 
Mizuno Toshiro, Yamaha Etsuro, Wakahara Masami, Kuroiwa Atsushi, Takeda Hiroyuki (1996): Mesoderm induction in zebrafish. Nature, 383, 131-132  https://doi.org/10.1038/383131a0
 
Nakagawa Masahiro, Kobayashi Toru, Ueno Koichi (2002): Production of germline chimera in loach (Misgurnus anguillicaudatus) and proposal of new method for preservation of endangered fish species. Journal of Experimental Zoology, 293, 624-631  https://doi.org/10.1002/jez.10184
 
Newport John, Kirschner Marc (1982): A major developmental transition in early xenopus embryos: II. control of the onset of transcription. Cell, 30, 687-696  https://doi.org/10.1016/0092-8674(82)90273-2
 
Okutsu T., Shikina S., Kanno M., Takeuchi Y., Yoshizaki G. (): Production of Trout Offspring from Triploid Salmon Parents. Science, 317, 1517-1517  https://doi.org/10.1126/science.1145626
 
Oprea D., Marica N., Costache M. (2014): Research considering embryonic development of pikeperch (Sander lucioperca) under artificial-controlled spawning conditions. Journal of Animal Science and Biotechnology, 47, 229–234.
 
Saito Taiju, Goto-Kazeto Rie, Kawakami Yutaka, Nomura Kazuharu, Tanaka Hideki, Adachi Shinji, Arai Katsutoshi, Yamaha Etsuro, Klymkowsky Michael (2011): The Mechanism for Primordial Germ-Cell Migration Is Conserved between Japanese Eel and Zebrafish. PLoS ONE, 6, e24460-  https://doi.org/10.1371/journal.pone.0024460
 
Schlumberger O., Proteau J.-P. (1996): Reproduction of pike-perch (Stizostedion lucioperca) in captivity. Journal of Applied Ichthyology, 12, 149-152  https://doi.org/10.1111/j.1439-0426.1996.tb00080.x
 
Takeuchi Yutaka, Yoshizaki Goro, Takeuchi Toshio (2001): Production of germ-line chimeras in rainbow trout by blastomere transplantation. Molecular Reproduction and Development, 59, 380-389  https://doi.org/10.1002/mrd.1044
 
Tsai Hsin-Yuan, Chang Mariann, Liu Shih-Chieh, Abe Gembu, Ota Kinya G. (2013): Embryonic development of goldfish ( Carassius auratus ): A model for the study of evolutionary change in developmental mechanisms by artificial selection. Developmental Dynamics, 242, 1262-1283  https://doi.org/10.1002/dvdy.24022
 
Wakamatsu Y., Ozato K., Hashimoto H., Kinoshita M., Sakaguchi M., Iwamatsu T. (1993): Generation of germ-line chimeras in medaka (Oryzias latipes). Molecular Marine Biology and Biotechnology, 2, 325–332.
 
Yamaha Etsuro, Mizuno Toshiro, Hasebe Yutaka, Takeda Hiroyuki, Yamazaki Fumio (1998): Dorsal specification in blastoderm at the blastula stage in the goldfish, Carassius auratus. Development, Growth and Differentiation, 40, 267-275  https://doi.org/10.1046/j.1440-169X.1998.t01-1-00002.x
 
Yamaha Etsuro, Mizuno Toshiro, Matsushita Ken, Hasebe Yutaka (1999): Developmental Staging in Goldfish during the Pre-gastrula Stage.. NIPPON SUISAN GAKKAISHI, 65, 709-717  https://doi.org/10.2331/suisan.65.709
 
Yamaha E., Kazama-Wakabayashi M., Otani S., Fujimoto T., Arai K. (2001): Germ-line chimera by lower part blastoderm transplantation between diploid goldfish and triploid crucian carp. Genetica, 111, 227–236. https://doi.org/10.1023/A:1013780423986
 
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. https://doi.org/10.1023/A:1026061828744
 
Yamaha Etsuro, Saito Taiju, Goto-Kazeto Rie, Arai Katsutoshi (2007): Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. Journal of Sea Research, 58, 8-22  https://doi.org/10.1016/j.seares.2007.02.003
 
Yoon C., Kawakami K., Hopkins N. (1997): Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development, 124, 3157–3165.
 
download PDF

© 2019 Czech Academy of Agricultural Sciences