Interspecific gynogenesis induction in Siberian sturgeon (Acipenser baerii ) using heterologous sperm

Document Type : Research Paper

Authors

1 Scientific Member in Genetics and Biotechnology Department, International Sturgeon Research Institute, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Rasht, Iran

2 Assistant Professor in Genetics and Biotechnology Department, International Sturgeon Research Institute, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Rasht, Iran

3 Professor in Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran

4 - Associate Professor in Genetics and Biotechnology Department, International Sturgeon Research Institute, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Rasht, Iran

5 M.Sc. in Fisheries, Aquaculture Department, International Sturgeon Research Institute, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Rasht, Iran

6 M.Sc. in Fisheries, Health and Disease Department, International Sturgeon Research Institute, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Rasht, Iran

10.22124/japb.2021.20693.1439

Abstract

Siberian sturgeon (Acipenser baerii) grows rapidly in breeding ponds. Gynogenesis is a suitable technique for producing sturgeon female sex. The aim of this study was to establish female sex in Siberian sturgeon using induction of gynogenesis. The sperm of Persian sturgeon (Acipenser persicus) was genetically inactivated by UV radiation at a dose of 8514 J/m2. In this case, sperm with 40% motility were combined with Siberian sturgeon oocytes and in 2°C cold shock for 30 minutes, 10 minutes after activity, gynogenic progeny were created. Fertilization rate was 44.5% (control hybrid 62%) and hatching rate was 19.8% (control hybrid 40.5%). Purely maternal heritability in gynogeneic progeny was confirmed using microsatellite markers. By achieving the biotechnique of sperm production with inactivated DNA of Persian sturgeon, it is possible to prevent the risk of extinction and protect other sturgeon by inducing gynogenesis.

Keywords


حسن‌زاده صابر م.، ذوالقرنین ح.، سالاری علی‌آبادی م.ع.، یزدانی ساداتی م.ع. و یارمحمدی م. 1398. ایجاد جنس نر تاس‌ماهی استرلیاد (Acipenser ruthenus) با به کارگیری اسپرم هترولوگ غیرفعال در القای گاینوژنز. فیزیولوژی و بیوتکنولوژی آبزیان، 7(4): 135-105.
کهنه‌شهری م. و آذری تاکامی ق. 1353. تکثیر و پرورش ماهیان خاویاری. انتشارات دانشگاه تهران. 281ص.
Billard R., Cosson J. and Crim L.W. 1993. Motility of fresh and aged halibut sperm. Aquatic Living Resources, 6(1): 67–75.
Cabrita E., Robles V. and Herraez P. 2008. Methods in Reproductive Aquaculture: Marine and Freshwater Species. CRC Press, USA. 574P.
Chebanov M. and Billard R. 2001. The culture of sturgeons in Russia: Production of juveniles for stocking and meat for human consumption. Aquatic Living Resources, 14(6): 375–381.
Chen S.L., Ji X.S., Shao C.W., Li W.L., Yang J.F., Liang Z., Liao X.L., Xu G.B., Xu Y. and Song W.T. 2012. Induction of mitogynogenetic diploids and identification of WW super-female using sex-specific SSR markers in half-smooth tongue sole (Cynoglossus semilaevis). Marine Biotechnology, 14(1): 120–128.
Chourrout D. 1980. Thermal induction of diploid gynogenesis and triploidy in the eggs of the rainbow trout (Salmo gairdneri Richardson). Reproduction Nutrition Developpement, 20(3): 727–733.
Dan C., Mei J., Wang D. and Gui J.F. 2013. Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish. International Journal of Biological Sciences, 9(10): 1043–1049.
Dietrich G.J., Szpyrka A., Wojtczak M., Dobosz S., Goryczko K. and Ciereszko A. 2005. Effects of UV irradiation and hydrogen peroxide on DNA fragmentation, motility and fertilizing ability of rainbow trout (Oncorhynchus mykiss) spermatozoa. Theriogenology, 64(8): 1809–1822.
Dorafshan S., Kalbassi M.R., Pourkazemi M. and Mojazi Amiri B. 2006. Optimization of UV irradiation for production of gynogenetic rainbow trout, Oncorhynchus mykiss: Emphasizing Hertwig effect and photo-reactivation. Iranian Journal of Fisheries Sciences, 6(1): 19–34.
Doroshov S.I., Moberg G.P. and Van Eenennaam J.P. 1997. Observations on the reproductive cycle of cultures white sturgeon, Acipenser transmontanus. Environmental Biology of Fishes, 48(1-4): 265–278.
Duplinsky P.D. 1982. Sperm motility of northern pike and chain pickerel at various pH values. Transactions of the American Fisheries Society, 111(6): 768–771.
Felip A., Piferrer F., Carrillo M. and Zanuy S. 1999. The relationship between the effects of UV light and thermal shock on gametes and the viability of early developmental stages in a marine teleost fish, the sea bass (Dicentrarchus labrax L.). Heredity, 83(4): 387–397.
Felip A., Zanuy S., Carrillo M. and Piferrer F. 2001. Induction of triploidy and gynogenesis in teleost fish with emphasis on marine species. Genetica, 111(1-3): 175–195.
Flynn S.R., Matsuoka M., Reith M., Martin-Robichaud D.J. and Benfey T.J. 2006. Gynogenesis and sex determination in shortnose sturgeon, Acipenser brevirostrum Lesuere. Aquaculture, 253(1-4): 721–727.
Fontana F. 1994. Chromosomal nucleolar organizer regions in            four sturgeon species as markers            of karyotype evolution in Acipenseriformes (Pisces). Genome, 37(5): 888–892.
Fontana F., Rossi R., Lanfredi M., Arlati G. and Bronzi P. 1997. Cytogenetic characterization of cell lines from three sturgeon species. Caryologia, 50(1): 91–95.
Fopp‐Bayat D. 2008. Inheritance of microsatellite loci in polyploid Siberian sturgeon (Acipenser baerii Brandt) based on uniparental haploids. Aquaculture Research, 39(16): 1787–1792.
Fopp-Bayat D. 2018. Genome manipulation and sex control in the Siberian sturgeon: An updated synthesis with regard to objectives, constraints and findings. P: 327–336. In: Williot P., Nonnotte G. and Chebanov M. (Eds.). The Siberian Sturgeon (Acipenser baerii, Brandt, 1869), Vol. 2: Farming. Springer, Cham, Switzerland.
Fopp‐Bayat D. and Ocalewicz K. 2015. Activation of the albino sterlet Acipenser ruthenus eggs by UV‐irradiated bester hybrid spermatozoa to provide gyno-genetic progeny. Reproduction in Domestic Animals, 50(4): 554–559.
Fopp-Bayat D., Hliwa P. and Ocalewicz K. 2018. Presence of gynogenetic males suggests a female heterogamety in sterlet Acipenser ruthenus L. Animal Reproduction Science, 189: 110–118.
Fopp-Bayat D., Kolman R. and Woznicki P. 2007. Induction of meiotic gynogenesis in sterlet (Acipenser ruthenus) using UV-irradiated bester sperm. Aquaculture, 264(1-4): 54–58.
Fopp-Bayat D., Ocalewicz K., Kucinski M., Jankun M. and Laczynska B. 2017. Disturbances in the ploidy level in the gynogenetic sterlet Acipenser ruthenus. Journal of Applied Genetics, 58(3): 373–380.
Grunina A.S., Skoblina M.N., Recoubratsky A.V., Kovalev K.V., Barmintseva A.E. and Goncharov B.F. 2011. Obtaining gynogenetic progeny of Siberian sturgeon (Acipenser baerii) using eggs matured and ovulated in vitro. Journal of Applied Ichthyology, 27(2): 701–705.
Hassanzadeh Saber M., Noveiri S.B., Pourkazemi M. and Yarmohammadi M. 2008. Induction of gynogenesis in stellate sturgeon (Acipenser stellatus Pallas, 1771) and its verification using microsatellite markers. Aquaculture Research, 39(14): 1483–1487.
Hillis D.M. and Moritz C. 1990. Molecular Taxonomy. Sinauer Associates Inc. Publishers, USA. 588P.
Hurvitz A., Jackson K., Degani G. and Levavi-Sivan B. 2007. Use of endoscopy for gender and ovarian stage determinations in Russian sturgeon (Acipenser gueldenstaedtii) grown in aquaculture. Aquaculture, 270(1-4): 158–166.
Ijiri K.I. and Egami N. 1980. Hertwig effect caused by UV-irradiation of sperm of Oryzias latipes (teleost) and its photoreactivation. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 69(2): 241–248.
Ji X.S., Tian Y.S., Yang J.F., Wu P.F., Jiang Y.L. and Chen S.L. 2010. Artificial gynogenesis in Cynoglossus semilaevis with homologous sperm and its verification using microsatellite markers. Aquaculture Research, 41(6): 913–920.
Lebeda I., Gazo I. and Flajshans M. 2014a. Chemical induction of haploid gynogenesis in sterlet Acipenser ruthenus. Czech Journal of Animal Science, 59: 310–318.
Lebeda I., Rodina M. and Flajshans M. 2014b. Optimization of sperm irradiation protocol for induced gynogenesis in Siberian sturgeon, Acipenser baerii. Aquaculture International, 22(2): 485–495.
Lebeda I., Steinbach C. and Flajshans M. 2018. Flow cytometry for assessing the efficacy of interspecific gynogenesis induction in sturgeon. Journal of Fish Biology, 92(6): 1819–1831.
Levanduski M.J. and Cloud J.G. 1988. Rainbow trout (Salmo gairdneri) semen: Effect of non-motile sperm on fertility. Aquaculture, 75(1-2): 171–179.
Linhart O., Mims S.D., Gomelsky B., Hiott A.E., Shelton W.L., Cosson J., Rodina M. and Gela D. 2000. Spermiation of paddlefish (Polyodon spathula, Acipenseriformes) stimulated with injection of LHRH analogue and carp pituitary powder. Aquatic Living Resources, 13(6): 455–460.
Ludwig A., Belfiore N.M., Pitra C., Svirsky V. and Jenneckens I. 2001. Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics, 158(3): 1203–1215.
Ma H.Y., Chen S.L. and Ji X.S. 2018. Sex‐specific markers, gynogenesis, and sex control in spotted halibut. P: 631–643. In: Wang H.P., Piferrer F., Chen S.L. and Shen Z.G. (Eds.). Sex Control in Aquaculture, Vol. 2. John Wiley and Sons, USA.
May B., Krueger C.C. and Kincaid H.L. 1997. Genetic variation at microsatellite loci in sturgeon: Primer sequence homology in Acipenser and Scaphirhynchus. Canadian Journal of Fisheries and Aquatic Sciences, 54(7): 1542–1547.
Meng Z., Liu X., Liu B., Hu P., Jia Y., Yang Z., Zhang H., Liu X. and Lei J. 2016. Induction of mitotic gynogenesis in turbot Scophthalmus maximus. Aquaculture, 451: 429–435.
Michalik O., Dobosz S., Zalewski T., Sapota M. and Ocalewicz K. 2015. Induction of gynogenetic and androgenetic haploid and doubled haploid development in the brown trout (Salmo trutta Linnaeus 1758). Reproduction in Domestic Animals, 50(2): 256–262.
Mims S.D., Shelton W.L., Linhart O. and Wang C. 1997. Induced meiotic gynogenesis of paddlefish Polyodon spathula. Journal of the World Aquaculture Society, 28(4): 334–343.
Mims S.D., Shelton W.L., Linhart O., Wang C., Gomelsky B. and Onders R.J. 2005. Application of a temperature‐dependent mitotic interval (τo) for induction of diploid meiotic gynogenetic paddlefish. North American Journal of Aquaculture, 67(4): 340–343.
Moan J. and Peak M.J. 1989. Effects of UV radiation on cells. Journal of Photochemistry and Photobiology (B), 4(1): 21–34.
Nowruzfashkhami M.R., Pourkazemi M. and Baradarannoveiri S. 2000. Chromosome study of Persian sturgeon Acipenser persicus B. Cytologia, 65: 197–202.
Ohta H., Shimma H. and Hirose K. 1995. Relationship between fertility and motility of cryopreserved spermatozoa of the amago salmon Oncorhynchus masou ishikawae. Fisheries Science, 61(5): 886–887.
Olaniyi W.A. and Omitogun O.G. 2014. Monosex fish production in fisheries management and its potentials for catfish aquaculture in Nigeria. P: 301–312. In: Behnassi M., Syomiti Muteng'e M., Ramachandran G. and Shelat K. (Eds.). Vulnerability of Agriculture, Water and Fisheries to Climate Change. Springer, Netherlands.
Omoto N., Maebayashi M., Adachi S., Arai K. and Yamauchi K. 2005. Sex ratios of triploids and gynogenetic diploids induced in the hybrid sturgeon, the bester (Huso huso female × Acipenser ruthenus male). Aquaculture, 245(1-4): 39–47.
Onozato H. 1982. The "Hertwig effect" and gynogenesis in chum salmon Oncorhynchus keta eggs fertilized with (60) Co gamma-ray irradiated milt (In Japanese with English summary). Bulletin of the Japanese Society of Scientific Fisheries, 48: 1237–1244.
Pan Z.J., Zhu C.K., Wang H., Chang G.L., Ding H.Y., Qiang X.G. and Yu X.S. 2017. Induction of meiotic gynogenesis in bagrid catfish (Pseudobagrus ussuriensis) with homologous sperm and its confirmation for female homogamety. Aquaculture Research, 48(11): 5659–5665.
Pandian T.J. 2011. Sex Determination in Fish. CRC Press, USA. 294P.
Piferrer F., Cal R.M., Gomez C., Alvarez-Blazquez B., Castro J. and Martinez P. 2004. Induction of gynogenesis in the turbot (Scophthalmus maximus): Effects of UV irradiation on sperm motility, the Hertwig effect and viability during the first 6 months of age. Aquaculture, 238(1-4): 403–419.
Pourkazemi M. 1996. Molecular and biochemical genetic analysis of sturgeon stocks from the South Caspian Sea. Ph.D. Thesis, Swansea University, Wales. 260P.
Recoubratsky A.V., Grunina A.S., Barmintsev V.A., Golovanova T.S., Chudinov O.S., Abramova A.B., Panchenko N.S. and Kupchenko S.A. 2003. Meiotic gynogenesis in the stellate and Russian sturgeons and sterlet. Russian Journal of Developmental Biology, 34(2): 92–101.
Ruban G. and Mugue N. 2022. Acipenser baerii. The IUCN Red List of Threatened Species 2022: Retrieved December 11, 2022, from https://dx.doi.org/10.2305/ IUCN.UK.2022-1.RLTS.T244A15 6718817.en.
Saber M.H. and Hallajian A. 2014. Study of sex determination system in ship sturgeon, Acipenser nudiventris using meiotic gynogenesis. Aquaculture International, 22(1): 273–279.
Saber M.H., Noveiri S.B., Pourkazemi M., Yazdani M., Ghoroghi A., Bahmani M., Pourdehghani M., Chakmehdouz F., Yarmohammadi M. and Nowruzfashkhami M. 2014. Induction of meiotic gynogenesis in ship sturgeon Acipenser nudiventris using UV-irradiated heterologous sperm. Journal of Applied Genetics, 55(2): 223–229.
Sinha R.P. and Hader D.P. 2002. UV-induced DNA damage and repair: A review. Photochemical and Photobiological Sciences, 1(4): 225–236.
Van Eenennaam A.L., Van Eenennaam J.P., Medrano J.F. and Doroshov S.I. 1999. Brief communication. Evidence of female heterogametic genetic sex determination in white sturgeon. Journal of Heredity, 90(1): 231–233.
Van Eenennaam A.L., Van Eenennaam J.P., Medrano J.F. and Doroshov S.I. 1996. Rapid verification of meiotic gynogenesis and polyploidy in white sturgeon (Acipenser transmontanus Richardson). Aquaculture, 147(3-4): 177–189.
Vasilyev V.P., Sokolov L.I. and Serebryakova Y.V. 1980. Karyotypes of the Siberian sturgeon, Acipenser baerii, of the Lena river and some aspects of karyotype evolution in Acipenseriformes. Journal of Ichthyology, 20(6): 37–45.
Welsh A.B., Blumberg M. and May B. 2003. Identification of microsatellite loci in lake sturgeon, Acipenser fulvescens, and their variability in green sturgeon, A. medirostris. Molecular Ecology Notes, 3(1): 47–55.
Williot P., Arlati G., Chebanov M., Gulyas T., Kasimov R., Kirschbaum F., Patriche N., Pavlovskaya L.P., Poliakova L., Pourkazemi M. and Kim Y. 2002. Status and management of Eurasian sturgeon: An overview. International Review of Hydrobiology, 87(5‐6): 483–506.
Wuertz S. Guralp H. Psenicka M. and Chebanov M. 2018. Sex determination in sturgeon. P: 645–668. In: Wang H.P., Piferrer F., Chen S.L. and Shen Z.G. (Eds.). Sex Control in Aquaculture, Vol. 2. John Wiley and Sons, USA.
Xiao J., Zou T.M., Chen L., Liu S.J., Zhang H., Long Y., Yan J.P., Zhao R.R., Tao M., Zhang C. and You C.P. 2011. Microsatellite analysis of different ploidy offspring of artificial gynogenesis in Cyprinus carpio. Journal of Fish Biology, 78(1): 150–165.
Xu J.H., You F., Yan B.L. and Zhang P.J. 2007. Effects of ultra-violet irradiation on sperm motility and diploid gynogenesis induction in large yellow croaker (Pseudosciaena crocea) undergoing cold shock. Aquaculture International, 15(5): 371–382.
Yuandong S., Min T., Shaojun L., Chun Z., Wei D., Jiamin S., Jing W., Chen Z., Yu L. and Yun L. 2007. Induction of gynogenesis in red crucian carp using spermatozoa of blunt snout bream. Progress in Natural Science, 17(2): 163–167.
Yuandong S.U.N., Zhang C., Shao-Jun L.I.U., Min T.A.O., Chen Z.E.N.G. and Yun L.I.U. 2006. Induction of gynogenesis in Japanese crucian carp (Carassius cuvieri). Acta Genetica Sinica, 33(5): 405–412.
Zou Y.C., Wei Q.W. and Pan G.B. 2011. Induction of meiotic gynogenesis in paddlefish (Polyodon spathula) and its confirmation using microsatellite markers. Journal of Applied Ichthyology, 27(2): 496–500.