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The yolk syncytial layer of loach, Misgurnus fossilis (Teleostei) during early development

Published online by Cambridge University Press:  04 July 2017

Ekaterina Kondakova ,
Irina Neklyudova  and
Vladimir Efremov
Ekaterina Kondakova*
Affiliation:
7/9 Universitetskaya nab., St Petersburg, 199034Russia
Irina Neklyudova
Affiliation:
1-12 Leninskie Gory, Moscow, 119991Russia
Vladimir Efremov*
Affiliation:
7/9 Universitetskaya nab., St Petersburg, 199034Russia
*
All correspondence to: Ekaterina Kondakova or Vladimir Efremov. 7/9 Universitetskaya nab., St Petersburg, 199034Russia. Tel: +79 219088092 E-mail: 23eak@mail.ru, katekondakova1989@gmail.com
All correspondence to: Ekaterina Kondakova or Vladimir Efremov. 7/9 Universitetskaya nab., St Petersburg, 199034Russia. Tel: +79 219088092 E-mail: 23eak@mail.ru, katekondakova1989@gmail.com
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Summary

The yolk syncytial layer (YSL) of Teleostei is a dynamic multifunctional temporary system. This paper describes the YSL structure of Misgurnus fossilis (Cobitidae) during its early developmental stages, studied using histological methods. YSL formation is prolonged. From the late blastula stage, the basal surface of the YSL is uneven and has protuberances, but becomes smoother during development. There are syncytial ‘islands’ with 1–2 yolk syncytial nuclei in the yolk mass. During epiboly, gastrulation and early segmentation, loach YSL is of different thickness in different regions along the dorso-ventral and antero-posterior axes of an embryo. The YSL is thickened in the dorsal region of gastrulae compared with the ventral region. Although the development of M. fossilis is similar to the development of zebrafish, there are important differences in YSL formation and organization that await further study and analysis. The study of YSL organization contributes to our knowledge of teleost developmental diversity and to the biology of temporary structures.

Keywords

BlastulaEpibolyGastrulaMisgurnus fossilisYolk syncytial layer
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 489 - 497
Copyright
Copyright © Cambridge University Press 2017 

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References

Aitkhozhin, M.A., Belitsina, N.V. & Spirin, A.S. (1964). Nucleic acids in the early stages of development of fish embryos (based on the loach Misgurnus fossilis). Biokhimiia (Moscow, Russia), 29, 169–75. [in Russian]Google ScholarPubMed
Alix, M., Chardard, D., Ledoré, Y., Fontaine, P. & Schaerlinger, B. (2015). An alternative developmental table to describe non-model fish species embryogenesis: application to the description of the Eurasian perch (Perca fluviatilis L. 1758) development. EvoDevo, 6, 1.CrossRefGoogle Scholar
Avraham-Davidi, I., Ely, Y., Pham, V.N., Castranova, D., Grunspan, M., Malkinson, G et al. (2012). ApoB-containing lipoproteins regulate angiogenesis by modulating expression of VEGF receptor 1. Nat. Med. 18, 967–73.Google Scholar
Bozhkova, V. & Voronov, D. (1997). Spatial-temporal characteristics of intercellular junctions in early zebrafish and loach embryos before and during gastrulation. Dev. Genes Evol., 207, 115–26.Google Scholar
Bruce, A.E. (2016). Zebrafish epiboly: Spreading thin over the yolk. Dev. Dynam., 245 244–58.CrossRefGoogle ScholarPubMed
Carvalho, L., Stühmer, J., Bois, J.S., Kalaidzidis, Y., Lecaudey, V. & Heisenberg, C.P. (2009). Control of convergent yolk syncytial layer nuclear movement in zebrafish. Development 136, 1305–15.Google Scholar
Carvalho, L. & Heisenberg, C.P. (2010). The yolk syncytial layer in early zebrafish development. Trends Cell Biol. 20, 586–592.CrossRefGoogle ScholarPubMed
Cherdantsev, V.G. & Tsvetkova, N.V. (2005). Dynamics and variability of early morphogenesis in the loach according to observations of individual developmental trajectories. Russ. J. Dev. Biol. 36, 171–80.Google Scholar
Cherdantsev, V.G. & Korvin-Pavlovskaya, E.G. (2016). Variability of quantitative morphogenetic parameters during early morphogenesis of the loach, Misgurnus fossilis L. Russ. J. Dev. Biol. 47, 49–62.Google Scholar
Chu, L.T., Fong, S.H., Kondrychyn, I., Loh, S.L., Ye, Z. & Korzh, V. (2012). Yolk syncytial layer formation is a failure of cytokinesis mediated by Rock1 function in the early zebrafish embryo. BiO 1, 747–53.Google Scholar
D'Amico, L.A. & Cooper, M.S. (2001). Morphogenetic domains in the yolk syncytial layer of axiating zebrafish embryos. Dev. Dynam. 222, 611–24.Google Scholar
Desnitskiy, A.G. (2015). On the features of embryonic cleavage in diverse fish species. Russ. J. Dev. Biol. 46, 326–32.Google Scholar
Finn, R.N. & Fyhn, H.J. (2010). Requirement for amino acids in ontogeny of fish. Aquac. Res., 41 684–716.CrossRefGoogle Scholar
Fuentes, R. & Fernández, J. (2010). Ooplasmic segregation in the zebrafish zygote and early embryo: pattern of ooplasmic movements and transport pathways. Dev. Dynam., 239, 2172–89.CrossRefGoogle ScholarPubMed
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, 747–55.Google Scholar
Fujimoto, T., Kataoka, T., Sakao, S., Saito, T., Yamaha, E. & Arai, K. (2006). Developmental stages and germ cell lineage of the loach (Misgurnus anguillicaudatus). Zool. Sci. 23, 977–89.CrossRefGoogle ScholarPubMed
Gasaryan, K.G., Hung, N.M., Neyfakh, A.A. & Ivanenkov, V.V. (1979). Nuclear transplantation in teleost Misgurnus fossilis L. Nature 280, 585–7.Google Scholar
Huttenhuis, H.B., Grou, C.P., Taverne-Thiele, A.J., Taverne, N. & Rombout, J.H. (2006). Carp (Cyprinus carpio L.) innate immune factors are present before hatching. Fish Shellfish Immun. 20, 586–96.Google Scholar
Ivanova-Kazas, OM. (1995). Evolutionary Embryology of Animals. St.-Petersburg: Nauka Publishers. 565 pp.Google Scholar
Jaroszewska, M. & Dabrowski, K. (2011). Utilization of yolk: transition from endogenous to exogenous nutrition in fish. Larval Fish Nutr. 183–218.Google Scholar
Jollie, W.P. & Jollie, L.G. (1967). Electron microscopic observations on the yolk sac of the spiny dogfish, Squalus acanthias . J. Ultrastruct. Res.,18, 102–26.Google Scholar
Kafiani, C.A., Timofeeva, M.J., Neyfakh, A.A., Melnikova, N.L. & Rachkus, J.A. (1969). RNA synthesis in the early embryogenesis of a fish (Misgurnus fossilis). Development 21, 295–308.Google Scholar
Kafiani, C.A., Akhalkatsi, R.G. & Gasaryan, K.G. (1973). Nuclear RNA polymerase activity and template efficiency of developing loach (Misgurnus fossilis) embryos. BBA-Nucl. Acids Protein Syn. 324, 133–42.Google ScholarPubMed
Kageyama, T. (1996). Polyploidization of nuclei in the yolk syncytial layer of the embryo of the medaka, Oryzias latipes, after the halt of mitosis. Dev. Growth Differ. 38, 119–27.Google Scholar
Kimble, M., Coursey, Y., Ahmad, N. & Hinsch, G.W. (2002). Behavior of the yolk nuclei during embryogenesis, and development of the midgut diverticulum in the horseshoe crab Limulus polyphemus . Invertebr. Biol. 121, 365–77.CrossRefGoogle Scholar
Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B. & Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dynam. 203, 253–310.Google Scholar
Kondakova, E.A. & Efremov, V.I. (2014). Morphofunctional transformations of the yolk syncytial layer during zebrafish development. J. Morphol. 275, 206–16.Google Scholar
Kondakova, E.A., Efremov, V.I. & Nazarov, V.A. (2016). Structure of the yolk syncytial layer in Teleostei and analogous structures in animals of the meroblastic type of development. Biol. Bull. 43, 208–15.Google Scholar
Korzh, V., Bajkova, O. & Dmitrevskaya, T. (1989). Microinjection of fluorescent dyes into loach (Misgurnus fossilis L.) embryos. 2. Morphology of giant nuclei of yolk syncytium. Ontogenez 20, 357–63. [in Russian]Google Scholar
Korzh, V., Dmitrevskaya, T. & Kononenko, V. (1990). Microinjection of fluorescent dyes into loach embryos. 3: Photometry of yolk syncytium giant nuclei. Ontogenez 21, 96–9. [in Russian]Google Scholar
Korzh, V. (2009). Before maternal–zygotic transition. . .there was morphogenetic function of nuclei. Zebrafish, 6, 295–302.Google Scholar
Korzh, V.P. & Minin, A.A. (2010). A short history of loach or why remember morphogenetic function of nuclei? The 50th anniversary of AA Neyfakh's discovery of the morphogenetic function of the nucleus. Russ. J. Dev. Biol. 41, 122–9.Google Scholar
Kostomarova, A.A. (1969). The differentiation capacity of isolated loach (Misgurnus fossilis L.) blastoderm. Development 22, 407–30.Google Scholar
Kostomarova, A.A. (1991). The loach Misgurnus fossilis . In Animal Species for Developmental Studies vol. 2 (eds Dettlaff, T.A. , Dettlaff & Vassetzky, Sergei G.), pp. 125–44. Springer USA.Google Scholar
Kunz, Y.W. (2004). Developmental Biology of Teleost Fishes. Dublin: Springer, 636 pp.CrossRefGoogle Scholar
Lentz, T.L. & Trinkaus, J.P. (1967). A fine structural study of cytodifferentiation during cleavage, blastula, and gastrula stages of Fundulus heteroclitus . J. Cell Biol. 32, 121–38.CrossRefGoogle ScholarPubMed
Lepage, S.E. & Bruce, A.E. (2010). Zebrafish epiboly: mechanics and mechanisms. Int. J. Dev. Biol. 54, 1213–28.Google Scholar
Mani-Ponset, L., Guyot, E., Diaz, J.P. & Connes, R. (1996). Utilization of yolk reserves during post-embryonic development in three teleostean species: the sea bream Sparus aurata, the sea bass Dicentrarchus labrax, and the pike-perch Stizostedion lucioperca . Mar. Biol. 126, 539–47.Google Scholar
Mayden, R.L., Chen, W.J., Bart, H.L., Doosey, M.H., Simons, A.M., Tang, K.L., . . . & Clements, M.D. (2009). Reconstructing the phylogenetic relationships of the earth's most diverse clade of freshwater fishes—order Cypriniformes (Actinopterygii: Ostariophysi): a case study using multiple nuclear loci and the mitochondrial genome. Mol. Phylogenet. Evol. 51, 500–14.Google Scholar
Nagai, H., Sezaki, M., Kakiguchi, K., Nakaya, Y., Lee, H.C., Ladher, R., Sasanami, T., Han, J.Y., Yonemura, S. & Sheng, G. (2015). Cellular analysis of cleavage-stage chick embryos reveals hidden conservation in vertebrate early development. Development 142, 1279–86.Google Scholar
Neklyudova, I.V., Korvin-Pavlovskaya, E.G. & Cherdantsev, V.G. (2007). Spatial-temporal dynamics of morphogenetic blastoderm potencies in early embryogenesis of the loach. Russ. J.Dev. Biol. 38, 294–309.Google Scholar
Neyfakh, A.A. (1959). X-ray inactivation of nuclei as a method for studying their function in the early development of fishes. Development 7, 173–92.CrossRefGoogle ScholarPubMed
Neyfakh, A. (1964). Radiation investigation of nucleo-cytoplasmic interrelations in morphogenesis and biochemical differentiation. Nature 201, 880–4.CrossRefGoogle ScholarPubMed
Padrós, F., Villalta, M., Gisbert, E. & Estévez, A. (2011). Morphological and histological study of larval development of the Senegal sole Solea senegalensis: an integrative study. J. Fish Biol. 79, 3–32.Google Scholar
Raicu, P. & Taisescu, E. (1972). Misgurnus fossilis, a tetraploid fish species. J. Hered. 63, 92–4.Google Scholar
Rozanova, N.V. & Bozhkova, V.P. (1995). Formation of the blastoderm basal layer in the loach and zebrafish embryos during the yolk syncytial layer development. Ontogenez 26, 437–45.Google Scholar
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–82.Google Scholar
Sleptzova, L.A., Neklyudova, I.V., Korvin-Pavlovskaya, E.G. & Burlakova, O.V. (2000). The Loach as an object of experimental embryological studies at the Department of Embryology. Russ. J. Dev. Biol. 31, 282–6.Google Scholar
Sire, M.F., Babin, P.J. & Vernier, J.M. (1994). Involvement of the lysosomal system in yolk protein deposit and degradation during vitellogenesis and embryonic development in trout. J. Exp. Zool. 269, 69–83.Google Scholar
Soin, S.G. 1981. A new classification of the structure of mature eggs of fishes according to the ratio of yolk to ooplasm. Sov. J. Dev. Biol. 12, 13–7.Google Scholar
Takesono, A., Moger, J., Farooq, S., Cartwright, E., Dawid, I.B., Wilson, S.W. & Kudoh, T. (2012). Solute carrier family 3 member 2 (Slc3a2) controls yolk syncytial layer (YSL) formation by regulating microtubule networks in the zebrafish embryo. Proc. Natl. Acad. Sci. USA 109, 3371–6.Google Scholar
Thomas, R.J. (1968). Yolk distribution and utililization during early development of a teleost embryo (Brachydanio rerio). Development 19, 203–15.CrossRefGoogle Scholar
Williams, D.W., Müller, F., Lavender, F.L., Orbán, L. & Maclean, N. (1996). High transgene activity in the yolk syncytial layer affects quantitative transient expression assays in zebrafish (Danio rerio) embryos. Transgenic Res. 5, 433–42.Google Scholar