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Ultrastructure of previtellogene oocytes in the neotenic cave salamander Proteus anguinus anguinus (Amphibia, Urodela, Proteidae)

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Abstract

Oogenesis in the neotenic, cave dwelling salamander Proteus anguinus anguinus has not been studied yet, and this study provides a detailed description of the early growth of the oocytes. Early previtellogene oocytes ranging from 100 to 600 µm in diameter were examined by light and transmission electron microscopy. The oocytes were divided into two stages based on size, color, and histology. Stage I oocytes can be identified by their transparent cytoplasm and a homogenous juxtanuclear mass, composed of numerous lipid droplets and mitochondria. Stage II oocytes are no longer transparent and have increased in diameter to 300– 600 µm, and many cortical alveoli differing in size have appeared. The common and most predominant ultrastructural characteristics of both stages of previtellogene oocytes are extensive quantities of smooth membrane, numerous mitochondria, and lipid droplets, as well as abundant free ribosomes. Myeline-like structures and remarkable annulate lamellae of closely packed membrane stacks are also frequently observed. Previtellogenic oocytes are the most predominant oocytes in the ovaries of Proteus, and while they possess certain structural characteristics typical for other amphibians, some features are unique and could result from adaptation to the subterranean environment.

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References

  • Abdalla FC, Cruz-Landim C (2003) Some histological and ultrastructural aspects of oogenesis in Piaractus mesopotamicus Holmerg, 1887 (Teleostei). Braz J Morph Sci 20(1):3–10

    Google Scholar 

  • Aranzábal MCU (2003) The ovary and oogenesis. In: Sever DM (ed) Reproductive biology and phylogeny of urodela, vol 1, 1st edn. Science Publishers, Inc., USA, pp 133–150

    Google Scholar 

  • Browder LW, Erickson CA, Jeffrey WR (1980) Developmental biology, 3rd edn. Sunders College, Fort Worth

    Google Scholar 

  • Dumont JN (1972) Oogenesis in Xenopus laevis (Daudin) I. Stages in laboratory maintained animals. J Morph 136:153–180

    Article  CAS  PubMed  Google Scholar 

  • Fusco S, Filosa S, Motta C (1997) Previtellogenesis in Antarctic fishes: comparison with temperate species. Ital J Zool 64:209–214

    Article  Google Scholar 

  • Ganion LR (1991) Cytoplasmic distribution of poly(A)-containing RNA in developing Necturus maculosus oocytes with reference to annulate lamellae. Anat Rec 230(2):218–224

    Article  CAS  PubMed  Google Scholar 

  • Ghadially FN (1997) Ultrastructural pathology of the cell and matrix, 4th edn. Butterworth-Heinemann, Boston

    Google Scholar 

  • Gülsoy N (2007) Development of the yolk nucleus of previtellogenic oocytes in rainbow trout, Oncorhynchus mykiss, studied by light microscopy. JABS I 2:33–35

    Google Scholar 

  • Guraya SS (1962) The structure and function of the so-called yolk-nucleus in the oogenesis of birds. Quart J micr Sci 103:411–415

    Google Scholar 

  • Guraya SS (1965) A comparative study of fish (Channa maruleus) and amphibian (Bufo somaticus) oogenesis. Z zellforsch 65:662–700

    Article  CAS  PubMed  Google Scholar 

  • Juberthie C, Durand J, Dupuy M (1996) La Rreproduction des Protées (Proteus anguinus): Bilan de 35 ans D'elevage dans les grottes-laboratories de Moulis et D'aulignac. Mémoires de Biospéologie, Tome XXIII: 53–56

  • Kessel RG (1965) Intranuclear and cytoplasmic annulate lamellae in tunicate oocytes. J Cell Biol 24:471–487

    Article  CAS  PubMed  Google Scholar 

  • Kessel RG, Tung HN, Beams HW, Lin JJC (1986) Is the nuclear envelope a “generator” of membrane? Developmental sequences in cytomembrane elaboration. Cell Tissue Res 245:61–68

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Etkin LD (2005) RNA localization mechanisms in oocytes. J Cell Sci 118:269–282

    Article  CAS  PubMed  Google Scholar 

  • Langecker TG (2000) The effects of continuous darkness on cave ecology and caverniculous evolution. In: Culver DC et al (eds) Ecosystems of the world: subterranean ecosystems, 1st edn. Elsevier, Amsterdam, pp 135–157

    Google Scholar 

  • Ogielska M, Kotusz A (2004) Pattern and rate of ovary differentiation with reference to somatic development in anuran amphibians. J Morphol 259:41–54

    Article  PubMed  Google Scholar 

  • Patino R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57–70

    Article  CAS  Google Scholar 

  • Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques, 5th edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Techn 35:313–323

    CAS  PubMed  Google Scholar 

  • Sánchez SS, Villecco EI (2003) Oogenesis. In: Jamieson GM (ed) Reproductive biology and phylogeny of anura, vol 2, 1st edn. Science Publishers, Enfield, pp 27–71

    Google Scholar 

  • Sarasquete C, Cardenas S, Gonzales de Canales ML, Pascual E (2002) Oogenesis in the bluefin tuna, Thunnus thynnus L.: a histological and histochemical study. Histol Histopatol 17:775–788

    CAS  Google Scholar 

  • Semakova KN, Kiseleva EV (2003) Myelin-like structure as a possible source of the smooth endoplasmic reticulum in early amphibian oocytes. Tsitologiya 45:746–757

    CAS  Google Scholar 

  • Sharon R, Degani G, Warburg MR (1997) Oogenesis and the ovarian cycle in Salamandra salamandra infraimmaculata Mertens (Amphibia, Urodela, Salamandridae) in fringe areas of the taxon's distribution. J Morphol 231:149–160

    Article  Google Scholar 

  • Sket B (1997) Distribution of Proteus (Amphibia: Urodela: Proteidae) and its possible explanation. J Biogeogr 24:263–280

    Article  Google Scholar 

  • Sretarugsa P, Weerachatyanukul W, Chavadej J, Kruatrachue M, Sobhon P (2001) Classification of developing oocytes, ovarian development and seasonal variation in Rana tigerina. Sci Asia 27:1–14

    Article  Google Scholar 

  • Tabaler I (2008) Oogenesis in the olm (Proteus anguinus, Amphibia: Urodela, Proteidae). Graduation thesis, University in Ljubljana, Slovenia

  • Villeco EI, Aybar MJ, Sanchez Rierra AN, Sanchez SS (1999) Comparative study of vitelogenesis in the anuran amphibians Ceratophrys cranweelii (Leptodactilidae) and Bufo arenarum (Bufonidae). Zygote 7:11–19

    Article  Google Scholar 

  • Wallace RA, Selman K (1990) Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J Electron Microsc Tech 16(3):175–201

    Article  CAS  PubMed  Google Scholar 

  • Weakley BS (1966) Electron microscopy of the oocyte and granulose cells in the developing ovarian follicles of the golden hamster (Mesocricetus auratus). J Anat 100(3):503–534

    CAS  PubMed  Google Scholar 

  • Zamboni L (1970) Ultrastructure of mammalian oocytes and ova. Biol Reprod Suppl 2:44–63

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This research was supported by the Ministry of Higer Education, Science and Technology, Republic of Slovenia, grant no. P1-0184.

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The authors declare that they have no conflict of interest.

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Correspondence to Lilijana Bizjak Mali.

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Mali, L.B., Bulog, B. Ultrastructure of previtellogene oocytes in the neotenic cave salamander Proteus anguinus anguinus (Amphibia, Urodela, Proteidae). Protoplasma 246, 33–39 (2010). https://doi.org/10.1007/s00709-010-0117-9

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  • DOI: https://doi.org/10.1007/s00709-010-0117-9

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