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

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Supplementary files

Supplementary Files
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1. JATS XML
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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