Cite this paper:
Jingjing SONG, Haiyi WU, Kaikai LIU, Wendan CHI, Shanshan GE, Zhipeng ZHANG, Mingqi WANG, Yi YU, Daode YU. Observation and analysis of morphology abnormalities in development of Oryzias melastigma embryos[J]. Journal of Oceanology and Limnology, 2021, 39(4): 1485-1499

Observation and analysis of morphology abnormalities in development of Oryzias melastigma embryos

Jingjing SONG1, Haiyi WU1, Kaikai LIU1, Wendan CHI1, Shanshan GE1, Zhipeng ZHANG2, Mingqi WANG2, Yi YU3, Daode YU1
1 Healthy Mariculture Engineering Research Center of Shandong Province, Marine Science Research Institute of Shandong Province, Qingdao 266104, China;
2 Tianjin Research Institute for Water Transport Engineering, Ministry of Transport, Tianjin 300456, China;
3 Ocean University of China, Qingdao 266100, China
Abstract:
Fish embryos are widely used as models in toxicology, drug development, and human disease research because of their high sensitivity, observability, and operability, providing the basis for an in-depth understanding of the embryogenesis. Increasing studies have indicated that birth defects are hereditary. In this study, we used Oryzias melastigma as a model to conduct a study of 185-day embryogenesis and observed self-induced non-pathological abnormal embryogenesis. O. melastigma experienced pre-puberty stage, adolescence stage, and senescence stage, and individuals produced up to 102 eggs per day. However, the fecundity was markedly reduced during the senescent stage. During the active egg and blastodisc stages, pseudo-fertilization and pseudo-blastocysts were observed. During cleavage at the 4-to 32-cell stages, we observed blastomeres separation or dislocation. Excessively separated blastomeres formed double blastoderms, eventually resulting in conjoined twins. During the blastula stage, we observed abnormally increased cell volume, narrowed and elongated blastocysts, and abnormally coated blastoderms. At the organogenesis stage, we observed abnormal numbers of Kupffer's vesicles and conjoined twins. Abnormality in the location and number of oil droplets were observed in various development stages. Abnormal development was more commonly observed in fertilized eggs produced by broodstock in prepuberty or senescence stages, which is probably related to the age of fish and the egg quality. This study can provide the materials for comparative analysis in toxicological and molecular studies of O. melastigma, and may provide evidence for other economic fish that produce sticky eggs.
Key words:    marine fish model|abnormal embryogenesis|blastomeres separation|Kupffer's vesicle|conjoined twins   
Received: 2020-06-10   Revised: 2020-08-02
Tools
PDF (6344 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Jingjing SONG
Articles by Haiyi WU
Articles by Kaikai LIU
Articles by Wendan CHI
Articles by Shanshan GE
Articles by Zhipeng ZHANG
Articles by Mingqi WANG
Articles by Yi YU
Articles by Daode YU
References:
Arbuatti A, Salda L D, Romanucci M. 2011. Histological observations on conjoined twins occurring among a captive-bred wild line of Poecilia wingei (Poeser, Kempkes & Isbrücker). Journal of Fish Diseases, 34(4):319-321, https://doi.org/10.1111/j.1365-2761.2011.01239.x.
Arezo M J, Pereiro L, Berois N. 2005. Early development in the annual fish Cynolebias viarius. Journal of Fish Biology, 66(5):1 357-1 370, https://doi.org/10.1111/j.0022-1112.2005.00688.x.
Bian X, Zhang X, Sakurai Y, Jin X, Gao T, Wan R, Yamamoto J. 2014. Temperature-mediated survival, development and hatching variation of Pacific cod Gadus macrocephalus eggs. Journal of Fish Biology, 84(1):85-105, https://doi.org/10.1111/jfb.12257.
Bo J, Cai L, Xu J H, Wang K J, Au D W T. 2011. The marine medaka Oryzias melastigma-A potential marine fish model for innate immune study. Marine Pollution Bulletin, 63(5-12):267-276, https://doi.org/10.1016/j.marpolbul.2011.05.014.
Bobe J, Labbé C. 2010. Egg and sperm quality in fish. General and Comparative Endocrinology, 165(3):535-548, https://doi.org/10.1016/j.ygcen.2009.02.011.
Brooks S, Tyler C R, Sumpter J P. 1997. Egg quality in fish:what makes a good egg? Reviews in Fish Biology and Fisheries, 7(4):387-416.
Brummett A R, Dumont J N. 1978. Kupffer's vesicle in Fundulus heteroclitus:a scanning and transmission electron microscope study. Tissue and Cell, 10(1):11-22, https://doi.org/10.1016/0040-8166(78)90003-4.
Chen Y, Wang X J, Ran H Y, Lin Y. 2016. Developmental stages of a marine model fish-medaka Oryzias melastigma. Oceanologia et Limnologia Sinica, 47(1):71-81. (in Chinese with English abstract)
Domínguez-Castanedo O, Valdesalici S, Rosales-Torres A M. 2018. Reproductive biology of annual killifishes and its relationship with embryonic survival during diapause:Millerichthys robustus (Cyprinodontiformes:Cynolebiidae) as an integrative model. Journal of Applied Ichthyology, 34(4):793-800, https://doi.org/10.1111/jai.13623.
Du R B, Wang Y Q, Jiang H B, Liu L M, Wang M J, Li T B, Zhang S B. 2010. Embryonic and larval development in barfin flounder Verasper moseri (Jordan and Gilbert).Chinese Journal of Oceanology and Limnology, 28(1):18-25, https://doi.org/10.1007/s00343-010-9251-7.
Duangkaew R, Kezuka F, Ichida K, Boonanuntanasarn S, Yoshizaki G. 2020. Aging- and temperature-related activity of spermatogonial stem cells for germ cell transplantation in medaka. Theriogenology, 155:213-221, https://doi.org/10.1016/j.theriogenology.2020.05.049.
Faria A M, Filipe S, Lopes A F, Oliveira A P, Gonçalves E J, Ribeiro L. 2017. Effects of high pCO2 on early life development of pelagic spawning marine fish. Marine and Freshwater Research, 68(11):2 106-2 114, https://doi.org/10.1071/mf16385.
Gore A V, Pillay L M, Galanternik M V, Weinstein B M. 2018.The zebrafish:a fintastic model for hematopoietic development and disease. Wiley Interdisciplinary Reviews:Developmental Biology, 7(3):e312, https://doi.org/10.1002/wdev.312.
Hand S C, Denlinger D L, Podrabsky J E, Roy R. 2016.Mechanisms of animal diapause:recent developments from nematodes, crustaceans, insects, and fish. American Journal of Physiology Regulatory, Integrative and Comparative Physiology, 310(11):R1193-R1211, https://doi.org/10.1152/ajpregu.00250.2015.
Hong H Z, Li D M, Shen R, Wang X H, Shi D L. 2014.Mechanisms of hexabromocyclododecanes induced developmental toxicity in marine medaka (Oryzias melastigma) embryos. Aquatic Toxicology, 152:173-185, https://doi.org/10.1016/j.aquatox.2014.04.010.
Hu C K, Brunet A. 2018. The African turquoise killifish:a research organism to study vertebrate aging and diapause.Aging Cell, 17(3):e12757, https://doi.org/10.1111/acel.12757.
Ishibashi H, Matsumura N, Hirano M, Matsuoka M, Shiratsuchi H, Ishibashi Y, Takao Y, Arizono K. 2004. Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquatic Toxicology, 67(2):167-179, https://doi.org/10.1016/j.aquatox.2003.12.005.
Ishigaki M, Kawasaki S, Ishikawa D, Ozaki Y. 2016. Nearinfrared spectroscopy and imaging studies of fertilized fish eggs:in vivo monitoring of egg growth at the molecular level. Scientific Reports, 6(1):20066, https://doi.org/10.1038/srep20066.
Iwamatsu T. 2004. Stages of normal development in the medaka Oryzias latipes. Mechanisms of Development, 121(7-8):605-618, https://doi.org/10.1016/j.mod.2004.03.012.
Kraeussling M, Wagner T U, Schartl M. 2011. Highly asynchronous and asymmetric cleavage divisions accompany early transcriptional activity in pre-blastula medaka embryos. PLoS One, 6(7):e21741, https://doi.org/10.1371/journal.pone.0021741.
Kreiling J A, Prabhat, Williams G, Creton R. 2007. Analysis of Kupffer's vesicle in zebrafish embryos using a cave automated virtual environment. Developmental Dynamics, 236(7):1 963-1 969, https://doi.org/10.1002/dvdy.21191.
Kyriakis D, Kanterakis A, Manousaki T, Tsakogiannis A, Tsagris M, Tsamardinos I, Papaharisis L, Chatziplis D, Potamias G, Tsigenopoulos C S. 2019. Scanning of genetic variants and genetic mapping of phenotypic traits in gilthead sea bream through ddRAD sequencing.Frontiers in Genetics, 10:675, https://doi.org/10.3389/fgene.2019.00675.
Laale H W. 1984. Polyembryony in teleostean fishes:double monstrosities and triplets. Journal of Fish Biology, 24(6):711-719, https://doi.org/10.1111/j.1095-8649.1984.tb04842.x.
Laale H W. 1985. Kupffer's vesicle in Brachydanio rerio:multivesicular origin and proposed function in vitro.Canadian Journal of Zoology, 63(10):2 408-2 415, https://doi.org/10.1139/z85-356.
Lanteri G, Macrì F, Marino F, Caracappa S, Mazzullo G. 2013.A rare case of deradelphus cephalo-thoracoomphalopagus in lamb. Anatomia, Histologia, Embryologia, 42(5):394-397, https://doi.org/10.1111/ahe.12017.
Levels P J, Denucé J M. 1988. Intrinsic variability in the frequency of embryonic diapauses of the annual fish Nothobranchius korthausae, regulated by light:dark cycle and temperature. Environmental Biology of Fishes, 22(3):211-224, https://doi.org/10.1007/bf00005382.
Mendieta-Serrano M A, Schnabel D, Lomelí H, Salas-Vidal E. 2013. Cell proliferation patterns in early zebrafish development. The Anatomical Record, 296(5):759-773, https://doi.org/10.1002/ar.22692.
Navis A, Marjoram L, Bagnat M. 2013. Cftr controls lumen expansion and function of Kupffer's vesicle in zebrafish.Development, 140(8):1 703-1 712, https://doi.org/10.1242/dev.091819.
Negrín-Báez D, Navarro A, Lee-Montero I, Soula M, Afonso J M, Zamorano M J. 2015. Inheritance of skeletal deformities in gilthead seabream (Sparus aurata)-lack of operculum, lordosis, vertebral fusion and LSK complex. Journal of Animal Science, 93(1):53-61, https://doi.org/10.2527/jas.2014-7968.
Okabe N, Xu B, Burdine R D. 2008. Fluid dynamics in zebrafish Kupffer's vesicle. Developmental Dynamics, 237(12):3 602-3 612, https://doi.org/10.1002/dvdy.21730.
Olivier N, Luengo-Oroz M A, Duloquin L, Faure E, Savy T, Veilleux I, Solinas X, Débarre D, Bourgine P, Santos A, Peyriéras N, Beaurepaire E. 2010. Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science, 329(5994):967-971, https://doi.org/10.1126/science.1189428.
Riesco M F, Valcarce D G, Martínez-Vázquez J M, Robles V. 2019. Effect of low sperm quality on progeny:a study on zebrafish as model species. Scientific Reports, 9(1):11 192, https://doi.org/10.1038/s41598-019-47702-7.
Scholz S, Gutzeit H O. 2000.17-α-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquatic Toxicology, 50(4):363-373, https://doi.org/10.1016/s0166-445x(00)00090-4.
Smith D J, Montenegro-Johnson T D, Lopes S S. 2014.Organized chaos in Kupffer's vesicle:how a heterogeneous structure achieves consistent left-right patterning. Bioarchitecture, 4(3):119-125, https://doi.org/10.4161/19490992.2014.956593.
Spencer R. 1992. Conjoined twins:theoretical embryologic basis. Teratology, 45(6):591-602, https://doi.org/10.1002/tera.1420450604.
Spencer R. 2001. Parasitic conjoined twins:External, internal(fetuses in fetu and teratomas), and detached (acardiacs).Clinical Anatomy, 14(6):428-444, https://doi.org/10.1002/ca.1079.
Wang Y H, Liu H J, Yu D D, Li Y Q, Guan S G, Liu Y. 2017.Observation of embryonic development of marine medaka Oryzias melastigma. Marine Sciences, 41(6):18-25. (in Chinese with English abstract)
Wilkinson R N, van Eeden F J M. 2014. The zebrafish as a model of vascular development and disease. Progress in Molecular Biology and Translational Science, 124:93-122, https://doi.org/10.1016/b978-0-12-386930-2.00005-7.
Wittbrodt J, Shima A, Schartl M. 2002. Medaka-a model organism from the Far East. Nature Reviews Genetics, 3(1):53-64, https://doi.org/10.1038/nrg704.
Xiao Z Z, Yu D D, Zhang X F, Xu S H, Ma D Y, Li J. 2008. Biological study on the early life history of barfin flound(Verasper moseri)-morphological & ecological characteristics of fertilized ova and the embryonic development of barfin flounder. Marine Sciences, 32(2):17-21. (in Chinese with English abstract)
Yu D D, Liu M, Liu H J, Jiang Y R, Guan S G. 2014. The embryonic development of Gadus macrocephalus Tilesius. Marine Sciences, 38(3):80-86. (in Chinese with English abstract)
Yu R M K, Chen E X H, Kong R Y C, Ng P K S, Mok H O L, Au D W T. 2006. Hypoxia induces telomerase reverse transcriptase (TERT) gene expression in non-tumor fish tissues in vivo:the marine medaka (Oryzias melastigma) model. BMC Molecular Biology, 7(1):27, https://doi.org/10.1186/1471-2199-7-27.
Yusupov R R. 2016. Embryonic and larval development of the Pacific cod Gadus macrocephalus from Taui Bay, northern Sea of Okhotsk. Russian Journal of Marine Biology, 41(7):580-591, https://doi.org/10.1134/s106307401507007x.
Zhu Z Y. 1982. Embryonic development of Clarias fuscus(Teleostei, Siluriformes). Acta Hydrobiologica Sinica, 7(4):445-454. (in Chinese with English abstract)
Copyright © Haiyang Xuebao