Dynamics of ultrastructural changes in the yolk syncytial layer and its microenvironment during gastrulation and early postembryonic development of Hemichromis Bimaculatus

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Abstract

BACKGROUND: In fish embryogenesis, the yolk sac is the critical provisional organ, actively functioning during the embryonic and early postembryonic stages. Its primary role is trophic, facilitated in Teleostei by a specialized structure — the yolk syncytial layer (YSL). Ultrastructural transformations of this layer during gastrulation and early postembryonic development, as well as its interaction with migrating muscle fibers and melanophores, are probably necessary for the efficient use of nutrients by the developing embryo. The yolk sac’s role in the embryogenesis of Hemichromis bimaculatus may extend beyond current conceptions.

AIM: To study the structural organization of the Jewel Cichlid (H. bimaculatus) yolk sac during the embryonic and early postembryonic development.

MATERIALS AND METHODS: The research was involved 22 embryos and larvae of H. bimaculatus from 1 to 7 days after egg laying. The morphological features of the yolk sac were studied using light and transmission electron microscopy.

RESULTS: By day 2, the yolk sac was separated from the embryo by the trunk fold. Its main structure was the YSL, containing numerous nuclei, microvilli, mitochondria and phagolysosomes. The morphological features of the YSL were similar to those of the placental symplastotrophoblast and indicated high functional activity. The yolk sac mesenchyme contained blood vessels, migrating melanophores, and muscle fibers. The periderm, covered with a special shell, fuunctioned as the primary skin of the embryo. The transition to exogenous nutrition in Jewel Cichlid larvae was accompanied by a significant decrease in yolk sac size with its subsequent involution.

CONCLUSIONS: The trophic function of the yolk sac in H. bimaculatus is mediated by the YSL, which, during gastrulation and postembryonic development, interacts with a number of structures present in the yolk sac wall. Migrating muscle fibers promote activation of yolk granules; accumulation of toxic metabolic products is associated with melanophores. The special structure of the periderm protects both the yolk sac and the embryo from external influences.

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About the authors

Natalya N. Dubinina

Novosibirsk State Medical University

Email: anna.dubinina05@gmail.com
ORCID iD: 0009-0000-6725-9445
SPIN-code: 6724-9437

Cand. Sci. (Biology), Assistant Professor Department of Histology, Embryology and Cytology

Russian Federation, 52 Krasny Prospect, 630091 Novosibirsk

Svetlana V. Aidagulova

Novosibirsk State Medical University

Email: asvetvlad@yandex.ru
ORCID iD: 0000-0001-7124-1969
SPIN-code: 5661-9765

Dr. Sci. (Biology), Professor , Head of the Laboratory of Cellular Biology and Fundamental Basis of Reproduction, Central scientific laboratory

Russian Federation, 52 Krasny Prospect, 630091 Novosibirsk

Svetlana V. Zalavina

Novosibirsk State Medical University

Author for correspondence.
Email: zalavinasv@mail.ru
ORCID iD: 0000-0003-3405-5993
SPIN-code: 8950-8517

MD, Dr. Sci. (Medicine), Assistant Professor

Russian Federation, 52 Krasny Prospect, 630091 Novosibirsk

References

  1. Ramos I, Machado E, Masuda H, et al. Open questions on the functional biology of the yolk granules during embryo development. Mol Reprod Dev. 2022;89(2):86–94. doi: 10.1002/mrd.23555
  2. Fleig R. Embryogenesis in mouth-breeding cichlids (Osteichthyes, Teleostei) structure and fate of the enveloping layer. Rouxs Arch Dev Biol. 1993;203(3):124–130. doi: 10.1007/BF00365051
  3. Concha ML, Reig G. Origin, form and function of extraembryonic structures in teleost fishes. Philos Trans R Soc Lond B Biol Sci. 2022;377(1865):20210264. doi: 10.1098/rstb.2021.0264
  4. Gorodilov YN, Melnikova ЕL. Embryonic development of the European smelt Osmerus eperlanus eperlanus (L.) (Neva population). Russian Journal of Marine Biology. 2006;32(3):173–185. EDN: HZJKFN
  5. Kaufman ZS. Embryologya ryb. Moscow: Agropromizdat; 1990. (In Russ.)
  6. Walzer DC, Schönenberger N. Ultrastructure and cytochemistry of the yolk syncytial layer in the alevin of trout (Salmo fario trutta L. and Salmo gairdneri R.) after hatching. Cell and Tissue Research. 1979;196(1):75–93. doi: 10.1007/BF00236349
  7. Ninhaus-Silveira A, Foresti F, de Azevedo A, et al. Structural and ultrastructural characteristics of the yolk syncytial layer in Prochilodus lineatus (Valenciennes, 1836) (Teleostei; Prochilodontidae). Zygote. 2007;15(3):267–271. doi: 10.1017/S0967199407004261
  8. Kondakova EA, Efremov VI, Nazarov VA. Structure of the yolk syncytial layer in Teleostei and analogous structures in animals of the meroblastic type of development. Biology Bulletin. 2016;43(3):208–215. EDN: WVBNMF doi: 10.1134/S1062359016030055
  9. Kondakova EA, Efremov VI, Bogdanova VA. Structure of the yolk syncytial layer in the larvae of whitefishes: A histological study. Russian Journal of Developmental Biology. 2017:48(3):176–184. EDN: XMWZJH doi: 10.1134/S1062360417030055
  10. Kondakova EA, Efremov VI, Kozin VV. Common and specific features of organization of the yolk syncytial layer of Teleostei as exemplified in Gasterosteus aculeatus L. Biology Bulletin. 2019:46(1):26–32. EDN: IYQFJO doi: 10.1134/S1062359019010023
  11. Herbomel P, Thisse B, Thisse C. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development. 1999;126(17):3735–3745. doi: 10.1242/dev.126.17.3735
  12. Sakaguchi T, Kikuchi Y, Kuroiwa A, et al. The yolk syncytial layer regulates myocardial migration by influencing extracellular matrix assembly in zebrafish. Development. 2006;133(20):4063–4072. doi: 10.1242/dev.02581
  13. Carter AM. IFPA senior award lecture: mammalian fetal membranes. Placenta. 2016;48 Suppl. 1:S21–S30. doi: 10.1016/j.placenta.2015.10.012
  14. Thowfeequ S, Srinivas S. Embryonic and extraembryonic tissues during mammalian development: shifting boundaries in time and space. Philos Trans R Soc Lond B Biol Sci. 2022;377(1865):20210255. doi: 10.1098/rstb.2021.0255
  15. Dubinina NN, Sklyanov YI, Popp EA, et al. Histogenetic parallels in the differentiation of yolk sac endoderm in some vertebrates. Morphology.2019:156(6):93. EDN: YRNTXT doi: 10.17816/morph.102018
  16. Peterson NG, Fox DT. Communal living: the role of polyploidy and syncytia in tissue biology. Chromosome Res. 2021;29(3–4):245–260. doi: 10.1007/s10577-021-09664-3
  17. Chu LT, Fong SH, Kondrychyn I, et al. Yolk syncytial layer formation is a failure of cytokinesis mediated by Rock1 function in the early zebrafish embryo. Biol Open. 2012;1(8):747–753. doi: 10.1242/bio.20121636
  18. Carvalho L, Stühmer J, Bois JS, et al. Control of convergent yolk syncytial layer nuclear movement in zebrafish. Development. 2009;136(8):1305–1315. doi: 10.1242/dev.026922
  19. Schwartz LM. Skeletal muscles do not undergo apoptosis during either atrophy or programmed cell death-revisiting the myonuclear domain hypothesis. Front Physiol. 2019;9:1887. doi: 10.3389/fphys.2018.01887
  20. Kondakova EA, Shkil FN, Efremov VI. Structure of the yolk syncytial layer during postembryonic development of Andinoacara rivulatus (Günther), 1860 (Cichlidae). Proceedings of the Zoological Institute RAS. 2019;323(4):523–532. EDN: NFAGNN doi: 10.31610/trudyzin/2019.323.4.523
  21. Jackson HE, Ingham PW. Control of muscle fibre-type diversity during embryonic development: The zebrafish paradigm. Mech Dev. 2013;130(9–10):447–457. doi: 10.1016/j.mod.2013.06.001
  22. Piesiewicz R, Krzystolik J, Korzelecka-Orkisz A, et al. Early ontogeny of cichlids using selected species as examples. Animals (Basel). 2024;14(8):1238. doi: 10.3390/ani14081238
  23. Mikulin AE. Functional significance of pigments and pigmentation in fish. Moscow: VNIRO; 2000. (In Russ.)

Supplementary files

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2. Fig. 1. Yolk sac of Hemichromis bimaculatus on the 2nd day after egg laying (hematoxylin and eosin staining): a — cross section of the embryo at the gastrula stage, general view; ×100; b — lamellar structure of the yolk; ×400; c — large nuclei of yolk syncytial layer; ×400. Here: ЖМ — yolk sac; Эм — embryo; ПЖ — yolk plates; Я — yolk syncytial layer nuclei. The tips mark the trunk fold.

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3. Fig. 2. Yolk sac of the Hemichromis bimaculatus on the 3rd day after egg laying: а — embryo cross section, general view; toluidine blue staining; ×100; b — yolk syncytial layer in contact with the yolk, parasagittal section; hematoxylin and eosin staining; ×400; c — fat droplets, yolk plates, yolk syncytial layer nuclei and migrating melanophores in the organ wall, cross section; toluidine blue staining; ×400; d — the ultrastructure (TEM ) of the yolk syncytial layer; ×4000. Here: ЖМ — yolk sac; Эм — embryo; ПЖ — yolk plates; ЖСС — yolk syncytial layer (cytoplasm); Я — yolk syncytial layer nucleus (indicated by an arrow); ЖК — fat droplet; Мф — melanophore.

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4. Fig. 3. The ultrastructure (TEM) of the yolk syncytial layer of the Hemichromis bimaculatus on the 4th day after egg laying (×4000): a — apical surface with microvilli; b — nucleus-containing part; c, d — yolk inclusions, phagolysosomes, myelin bodies and mitochondria in the cytoplasm. Here: ЖВ — yolk inclusions; ЯЖСС — yolk syncytial layer nucleus; Мв — microvilli; Мх — mitochondria; Фл — phagolysosomes; МТ — myelin bodies.

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5. Fig. 4. Structural elements of the Hemichromis bimaculatus yolk sac on days 4–5 after egg laying: a — periderm, parasagittal section; hematoxylin and eosin staining; ×400; b — melanophore ultrastructurе; ×4500; c — muscle fibers and melanophores on the organ surface, the cross section; toluidine blue staining; ×400; d — muscle fiber fragment; e, f — ultrastructurе of periderm cells; ×4000. Here: ЖМ — yolk sac; Я — cell nuclei; Мф — melanophore; Пе — periderm; П/ПМТ — striated muscle tissue; Мфбр — myofibril.

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6. Fig. 5. Yolk sac of the Hemichromis bimaculatus on the 5–7 day after egg laying: a — embryo cross section (5th day), general view; hematoxylin and eosin staining; ×100; b — yolk structure, parasagittal section; toluidine blue staining; ×400; c — embryo cross section (7th day), general view; hematoxylin and eosin staining; ×100; d — fragment of the ventral part of the embryo; hematoxylin and eosin staining; ×400. Here: ЖМ — yolk sac; ЯЖСС — YSS nuclei (indicated by arrows); Мф — melanophore (indicated by arrow); Пч — liver; Кш — embryonic intestine.

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7. Consent to the processing of personal data Dubinina

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