Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-25T01:54:07.778Z Has data issue: false hasContentIssue false
  • English
  • Français

Embryo manipulation in neotropical characiform fish: incubation system, anaesthetic, and PGC transplantation in Prochilodus lineatus

Published online by Cambridge University Press:  05 August 2022

Gabriella Braga Carvalho Open the ORCID record for Gabriella Braga Carvalho [Opens in a new window] ,
Geovanna Carla Zacheo Coelho ,
Andreoli Correia Alves Open the ORCID record for Andreoli Correia Alves [Opens in a new window] ,
Amanda Pereira Dos Santos Silva ,
Paulo Sérgio Monzani ,
José Augusto Senhorini Open the ORCID record for José Augusto Senhorini [Opens in a new window] ,
Norberto Castro Vianna  and
George Shigueki Yasui
Gabriella Braga Carvalho*
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil
Geovanna Carla Zacheo Coelho
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil
Andreoli Correia Alves
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil
Amanda Pereira Dos Santos Silva
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil
Paulo Sérgio Monzani
Affiliation:
Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil Institute of Bioscience, São Paulo State University, Botucatu, Brazil
José Augusto Senhorini
Affiliation:
Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil Institute of Bioscience, São Paulo State University, Botucatu, Brazil
Norberto Castro Vianna
Affiliation:
China Three Gorges Corporation Brazil, Chavantes, Brazil
George Shigueki Yasui
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil Laboratory of Fish Biotechnology, National Center for Research and Conservation of Continental Aquatic Biodiversity, Chico Mendes Institute of Biodiversity Conservation, Pirassununga, São Paulo, Brazil Institute of Bioscience, São Paulo State University, Botucatu, Brazil
*
Author for correspondence: Gabriella Braga Carvalho. Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil. Av. Prof. Orlando Marques de Paiva, 87, Cidade Universitária São Paulo, SP, Brazil. CEP: 05508–270. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Primordial germ cells transplantation is a unique approach for conservation and reconstitution of endangered fish species. This study aimed to establish techniques to culture dechorionated embryos in different incubation systems and also to determine anaesthetic concentration for fish recipients in the larval stage for subsequent primordial germ cell transplantation. Intact and dechorionated embryos were divided into three incubation systems: (1) a control group with manual replacement of the solution; (2) a closed environment with high oxygen with manual replacement of the solution; and (3) constant solution recirculation. This combination resulted in six treatments. For the evaluation of anaesthetics for larvae, the concentrations evaluated were 19.5 mM, 24.4 mM, 29.3 mM, and 34.2 mM of 2-phenoxyethanol. Anaesthesia concentration and recovery at different stages were evaluated. For transplantation, primordial germ cells of Astyanax altiparanae were transplanted into anaesthetised larvae (1 dph) of Prochilodus lineatus. Better results were obtained in the recirculation system for dechorionated embryos of P. lineatus for hatching (54.18%) and normal morphology (50.06%). The 2-phenoxyethanol anaesthetic with a dose of 29.3 mM resulted in shorter induction times, in addition to the recovery time between 5 and 10 min. By using this anaesthetic concentration at transplantation, GFP-positive cells were seen in two recipients, but the cells did not proliferate. This study established an effective incubation system for the development of the dechorionated embryo and determined an effective anaesthetic concentration for P. lineatus larvae. In addition, micromanipulation and transplantation of primordial germ cells in neotropical species were conducted for the first time.

Keywords

BiotechnologyDechorionated embryo and conservationMicromanipulation2-Phenoxyethanol
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 773 - 780
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bar, I., Smith, A., Bubner, E., Yoshizaki, G., Takeuchi, Y., Yazawa, R., Chen, B. N., Cummins, S. and Elizur, A. (2016). Assessment of yellowtail kingfish (Seriola lalandi) as a surrogate host for the production of southern bluefin tuna (Thunnus maccoyii) seed via spermatogonial germ cell transplantation. Reproduction, Fertility, and Development, 28(12), 2051–2064. doi: 10.1071/RD15136 CrossRefGoogle ScholarPubMed
Ciruna, B., Weidinger, G., Knaut, H., Thisse, B., Thisse, C., Raz, E. and Schier, A. F. (2002). Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proceedings of the National Academy of Sciences of the United States of America, 99(23), 14919–14924. doi: 10.1073/pnas.222459999 CrossRefGoogle ScholarPubMed
Cloud, J. G., Miller, W. H. and Levanduski, M. J. (1990). Cryopreservation of sperm as a means to store salmonid germ plasm and to transfer genes from wild fish to hatchery populations. Progressive Fish-Culturist, 52(1), 51–53. doi: 10.1577/1548-8640(1990)052<0051:COSAAM>2.3.CO;2 2.3.CO;2>CrossRefGoogle Scholar
Coelho, G. C. Z., Yo, I. S., Mira-López, T. M., Monzani, P. S., Arashiro, D. R., Fujimoto, T., Senhorini, J. A. and Yasui, G. S. (2019). Preparing a fish embryo (Prochilodus lineatus) for staging, chorion removal and PGC traceability. International Journal of Developmental Biology, 63(1–2), 57–65. doi: 10.1387/ijdb.180348gc CrossRefGoogle Scholar
De Siqueira-Silva, D. H., Saito, T., Dos Santos-Silva, A. P., Da Silva Costa, R., Psenicka, M. and Yasui, G. S. (2018). Biotechnology applied to fish reproduction: Tools for conservation. Fish Physiology and Biochemistry, 44(6), 1469–1485. doi: 10.1007/s10695–018–0506–0TSIDOU,CrossRefGoogle ScholarPubMed
Doitsidou, M., Reichman-Fried, M., Stebler, J., Köprunner, M., Dörries, J., Meyer, D. and Raz, E. (2002). Guidance of primordial germ cell migration by the chemokine SDF-1. Cell, 111(5), 647–659. doi: 10.1016/S0092–8674(02)01135-2 CrossRefGoogle ScholarPubMed
Food and Agriculture Organization. (2020). State of World Fisheries and Aquaculture. Food and Agriculture Organization of the United Nations, 210.Google Scholar
Farlora, R., Hattori-Ihara, S., Takeuchi, Y., Hayashi, M., Octavera, A., Alimuddin, Y. and G. (2014). Intraperitoneal germ cell transplantation in the Nile tilapia Oreochromis niloticus . Marine Biotechnology, 16, 309–320. doi: 10.1007/s10126–013–9551-y CrossRefGoogle ScholarPubMed
Hagedorn, M. and Kleinhans, F. W. (2000). Problems and prospects in cryopreservation of fish embryos. In Tiersch, T. R. and Mazik, P. M. (eds.), Cryopreservation in aquatic species (pp. 161–178). World Aquaculture Society.Google Scholar
Hattori, R. S., Yoshinaga, T. T., Katayama, N., Hattori-Ihara, S., Tsukamoto, R. Y., Takahashi, N. S. and Tabata, Y. A. (2019). Surrogate production of Salmo salar oocytes and sperm in triploid Oncorhynchus mykiss by germ cell transplantation technology. Aquaculture, 506, 238–245. doi: 10.1016/j.aquaculture.2019.03.037 CrossRefGoogle Scholar
Hohlenwerger, J. C., Eduardo Copatti, C., Cedraz Sena, A., David Couto, R., Baldisserotto, B., Heinzmann, B. M., Caron, B. O. and Schmidt, D. (2016). Could the essential oil of Lippia alba provide a readily available and cost-effective anaesthetic for Nile tilapia (Oreochromis niloticus)? Marine and Freshwater Behaviour and Physiology, 49(2), 119–126. doi: 10.1080/10236244.2015.1123869 CrossRefGoogle Scholar
Holt, W. V. and Pickard, A. R. (1999). Role of reproductive technologies and genetic resource banks in animal conservation. Reviews of Reproduction, 4(3), 143–150. doi: 10.1530/ror.0.0040143 CrossRefGoogle ScholarPubMed
Huang, C., Dong, Q., Walter, R. B. and Tiersch, T. R. (2004). Sperm cryopreservation of green swordtail Xiphophorus helleri, a fish with internal fertilization. Cryobiology, 48(3), 295–308. doi: 10.1016/j.cryobiol.2004.02.004 CrossRefGoogle ScholarPubMed
Köprunner, M., Thisse, C., Thisse, B. and Raz, E. (2001). A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes and Development, 15(21), 2877–2885. doi: 10.1101/gad.212401 CrossRefGoogle ScholarPubMed
Li, Q., Fujii, W., Naito, K. and Yoshizaki, G. (2017). Application of dead end-knockout zebrafish as recipients of germ cell transplantation. Molecular Reproduction and Development, 84(10), 1100–1111. doi: 10.1002/mrd.22870 CrossRefGoogle ScholarPubMed
MMA/ICMBIO. (2018). Livro vermelho da fauna Brasileira ameaçada de.extinção. 495 pp.Google Scholar
Morita, T., Kumakura, N., Morishima, K., Mitsuboshi, T., Ishida, M., Hara, T., Kudo, S., Miwa, M., Ihara, S., Higuchi, K., Takeuchi, Y. and Yoshizaki, G. (2012). Production of donor-derived offspring by allogeneic transplantation of spermatogonia in the yellowtail (Seriola quinqueradiata). Biology of Reproduction, 86(6), 176. doi: 10.1095/biolreprod.111.097873 CrossRefGoogle Scholar
Murray, M. J. (2002). Fish surgery. Seminars in Avian and Exotic Pet Medicine, 11(4), 246–257. doi: 10.1053/saep.2002.126571 CrossRefGoogle Scholar
Mylonas, C. C., Cardinaletti, G., Sigelaki, I. and Polzonetti-Magni, A. (2005). Comparative efficacy of clove oil and 2-phenoxyethanol as anesthetics in the aquaculture of European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) at different temperatures. Aquaculture, 246(1–4), 467–481. doi: 10.1016/j.aquaculture.2005.02.046 CrossRefGoogle Scholar
Nagasawa, K., Fernandes, J. M., Yoshizaki, G., Miwa, M. and Babiak, I. (2013). Identification and migration of primordial germ cells in Atlantic salmon, Salmo salar: characterization of vasa, dead end, and lymphocyte antigen 75 genes. Molecular Reproduction and Development, 80(2), 118–131. doi: 10.1002/mrd.22142 CrossRefGoogle ScholarPubMed
Ninhaus-Silveira, A., Foresti, F. and De Azevedo, A. (2006). Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiforme; Prochilodontidae). Zygote, 14(3), 217–229. doi: 10.1017/S096719940600373X CrossRefGoogle Scholar
Okutsu, T., Suzuki, K., Takeuchi, Y., Takeuchi, T. and Yoshizaki, G. (2006). Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. PNAS, 103, 4–5.CrossRefGoogle ScholarPubMed
Parodi, T. V., Cunha, M. A., Becker, A. G., Zeppenfeld, C. C., Martins, D. I., Koakoski, G., Barcellos, L. G., Heinzmann, B. M. and Baldisserotto, B. (2014). Anaesthetic activity of the essential oil of Aloysia triphylla and effectiveness in reducing stress during transport of albino and grey strains of silver catfish, Rhamdia quelen . Fish Physiology and Biochemistry, 40, 323–334. doi: 10.1007/s10695–013–9845-z CrossRefGoogle Scholar
Piva, L. H., De Siqueira-Silva, D. H., Goes, C. A. G., Fujimoto, T., Saito, T., Dragone, L. V., Senhorini, J. A., Porto-Foresti, F., Ferraz, J. B. S. and Yasui, G. S. (2018). Triploid or hybrid tetra: Which is the ideal sterile host for surrogate technology? Theriogenology, 108, 239–244. doi: 10.1016/j.theriogenology.2017.12.013 CrossRefGoogle ScholarPubMed
Rivers, N., Daly, J. and Temple-Smith, P. (2020). New directions in assisted breeding techniques for fish conservation. Reproduction, Fertility, and Development, 32(9), 807–821. doi: 10.1071/RD19457 CrossRefGoogle ScholarPubMed
Routray, P. (2020). Cryopreservation and storage of oocytes, embryos and embryonic cells of fish. In Cryopreservation of fish gametes (pp. 313–336). doi: 10.1007/978-981-15-4025-7_13. Springer.CrossRefGoogle Scholar
Saito, T., Pšenička, M., Goto, R., Adachi, S., Inoue, K., Arai, K. and Yamaha, E. (2014). The origin and migration of primordial germ cells in sturgeons. PLoS ONE, 9(2), e86861. doi: 10.1371/journal.pone.0086861 CrossRefGoogle ScholarPubMed
Saito, T., Goto-Kazeto, R., Kawakami, Y., Nomura, K., Tanaka, H., Adachi, S., Arai, K. and Yamaha, E. (2011). The mechanism for primordial germ-cell migration is conserved between Japanese eel and zebrafish. PLoS ONE, 6(9), e24460. doi: 10.1371/journal.pone.0024460 CrossRefGoogle ScholarPubMed
Saito, T., Goto-Kazeto, R. I. E., Fujimoto, T., Kawakami, Y., Arai, K. and Yamaha, E. (2010). Inter-species transplantation and migration of primordial germ cells in cyprinid fish. International Journal of Developmental Biology, 54(10), 1481–1486. doi: 10.1387/ijdb.103111ts CrossRefGoogle ScholarPubMed
Saito, T., Goto-Kazeto, R., Arai, K. and Yamaha, E. (2008). Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biology of Reproduction, 78(1), 159–166. doi: 10.1095/biolreprod.107.060038 CrossRefGoogle ScholarPubMed
Takeuchi, Y., Yoshizaki, G. and Takeuchi, T. (2003). Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biology of Reproduction, 69(4), 1142–1149. doi: 10.1095/biolreprod.103.017624 CrossRefGoogle ScholarPubMed
Takeuchi, Y., Yoshizaki, G. and Takeuchi, T. (2001). Production of germ-line chimeras in rainbow trout by blastomere transplantation. Molecular Reproduction and Development, 59(4), 380–389. doi: 10.1002/mrd.1044 CrossRefGoogle ScholarPubMed
Toni, C., Martos-Sitcha, J. A., Baldisserotto, B., Heinzmann, B. M., De Lima Silva, L., Martínez-Rodríguez, G. and Mancera, J. M. (2015). Sedative effect of 2-phenoxyethanol and essential oil of Lippia alba on stress response in gilthead sea bream (Sparus aurata). Research in Veterinary Science, 103, 20–27. doi: 10.1016/j.rvsc.2015.09.006 CrossRefGoogle Scholar
Winemiller, K. O., Agostinho, A. A. and Caramaschi, E. P. (2008). Fish ecology in tropical streams. In Dudgeon, D. (ed.) Tropical Stream Ecology (pp. 107–146). Elsevier/Academic Press, San Diego, CA.CrossRefGoogle Scholar
Yasui, G. S., Arias-Rodriguez, L., Fujimoto, T. and Arai, K. (2009). A sperm cryopreservation protocol for the loach Misgurnus anguillicaudatus and its applicability for other related species. Animal Reproduction Science, 116(3–4), 335–345. doi: 10.1016/j.anireprosci.2009.02.021 CrossRefGoogle ScholarPubMed
Yasui, G. S., Fujimoto, T., Sakao, S., Yamaha, E. and Arai, K. (2011). Production of loach (Misgurnus anguillicaudatus) germ-line chimera using transplantation of primordial germ cells isolated from cryopreserved blastomeres. Journal of Animal Science, 89(8), 2380–2388. doi: 10.2527/jas.2010-3633 CrossRefGoogle ScholarPubMed
Yasui, G. S., Senhorini, J. A., Shimoda, E., Pereira-Santos, M., Nakaghi, L. S. O., Fujimoto, T., Arias-Rodriguez, L. A. and Silva, L. A. (2015). Improvement of gamete quality and its short-term storage: an approach for biotechnology in laboratory fish. Animal, 9(3), 464–470. doi: 10.1017/S1751731114002511 CrossRefGoogle ScholarPubMed
Yasui, G. S., Nakaghi, L. S. O., Monzani, P. S., Nascimento, N. Fd, Pereira dos Santos, M., Goes, C. A. G., Porto-Foresti, F. and Senhorini, J. A. (2020). Triploidization in the streaked prochilod Prochilodus lineatus inferred by flow cytometry, blood smears and karyological approaches. Journal of Applied Ichthyology, 36(3), 336–341. doi: 10.1111/jai.14025 CrossRefGoogle Scholar
Yön, N. D. and Akbulut, C. (2015). Identification of primordial germ cells: Cytological, histological and immunohistochemical aspects. Brazilian Archives of Biology and Technology, 58(2), 222–228. doi: 10.1590/S1516-8913201500335 CrossRefGoogle Scholar
Yoshizaki, G., Takeuchi, Y., Kobayashi, T., Ihara, S. and Takeuchi, T. (2002). Primordial germ cells: The blueprint for a piscine life. Fish Physiology and Biochemistry, 26(1), 3–12. doi: 10.1023/A:1023388317621 CrossRefGoogle Scholar
Yoshizaki, G., Takeuchi, Y., Kobayashi, T. and Takeuchi, T. (2003). Primordial germ cell: A novel tool for fish bioengineering. Fish Physiology and Biochemistry, 28(1–4), 453–457. doi: 10.1023/B:FISH.0000030628.91607.2d CrossRefGoogle Scholar
Yoshizaki, G., Tago, Y., Takeuchi, Y., Sawatari, E., Kobayashi, T. and Takeuchi, T. (2005). Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in Salmonidae. Biology of Reproduction, 73(1), 88–93. doi: 10.1095/biolreprod.104.034249 CrossRefGoogle ScholarPubMed