Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-27T16:56:08.294Z Has data issue: false hasContentIssue false
  • English
  • Français

Fine structural observation on the oogenesis and vitellogenesis of the Chinese soft-shelled turtle (Pelodiseus sinensis)

Published online by Cambridge University Press:  09 July 2009

Hei Nainan ,
Yang Ping ,
Yang Yang ,
Liu Jinxiong ,
Bao Huijun ,
Liu Haili ,
Zhang Hui  and
Chen Qiusheng
Hei Nainan
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Yang Ping
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Yang Yang
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Liu Jinxiong
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Bao Huijun
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Liu Haili
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Zhang Hui
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
Chen Qiusheng*
Affiliation:
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, China. College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China.
*
All correspondence to: Chen Qiusheng. College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, China. Tel: +86 25 84395817. Fax: +86 25 84398699. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Fine structure observations were performed by means of electron microscopy on oogenesis and vitellogenesis and the special functions of follicular cells in the Chinese soft-shelled turtle (Pelodiseus sinensis). Histological examination of the ovary showed a well developed lacunae system containing fine granules, fibres or gelatiniform materials with one or two germinal beds dispersed on the dorsal surface of the ovarian cortex. The process of oogenesis comprised 10 consecutive phases according to the morphology of the yolk platelets, follicular cells and zona pellucida (ZP). Electron microscopy of vitellogenesis revealed some of the mitochondria gradually being transformed into yolk granules. In the advanced stage of vitellogenesis, large amounts of rough endoplasmic reticula, Golgiosomes and other cell organelles that are involved in synthesis and secretion were observed in follicular cells. The ZP was formed by microvilli, thus increasing the absorptive surface of the oocyte and facilitating transport of nutrients from the follicular epithelium to the ooplasm. This study demonstrated that the ovaries of members of the Testudinidae share more features with Archosaurs than with Squamates, indicating that these features were phylogenetically conserved in the Archosauria. The present observations suggest that the accumulation of yolk materials was controlled by the intrinsic and extrinsic pathways as well as by the activity of follicular cells. These results might also support a sibling relationship of the Testudinidae with the Archosauria and not with all extant reptiles.

Keywords

MicrostructureOogenesisPelodiseus sinensisUltrastructureVitellogenesis
Type
Research Article
Information
Zygote , Volume 18 , Issue 2 , May 2010 , pp. 109 - 120
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andreuccetti, P. (1992). An ultrastructural study of differentiation of pyriform cells and their contribution to oocyte growth in representative squamata. J. Morphol. 212, 1–11.CrossRefGoogle ScholarPubMed
Hedges, S.B. & Poling, L.L. (1999). A molecular phylogeny of reptiles. Science 283, 998–1001.CrossRefGoogle ScholarPubMed
Cai, Y.F., Li, J. & Chen, B.H. (1999). Folliculogenesis in Gekko swinhonis. Life Sci. Res. 3, 58–63.Google Scholar
Cai, Y.F., Liu, H.L. & Wang, G.L. (2004). Vitellogenesis of lizards in follicles. Chi. J. Anat. 27, 121–5.Google Scholar
Calderón, M.L., De Pérez, G.R. & Ramírez Pinilla, M.P. (2004). Morphology of the ovary of Caiman crocodilus (Crocodilia: Alligatoridae). Ann. Anat. 186, 13–24.CrossRefGoogle Scholar
Callebaut, M., Van Nassauw, L. & Harrison, F. (1997). Comparison between oogenesis and related ovarian structure in a reptile, Pseudemys scripta elegans (turtle) and in a bird Coturnix coturnix japonica (quail). Reprod. Nutr. 37, 233–52.CrossRefGoogle Scholar
Callebaut, M. (1988). The ovarian chordolacunar system in birds. Arch. Biol. (Bruxelles) 99, 1–15.Google Scholar
Chen, F.Y., Hua, T.M. & Chen, B.H. (1998). Studies on the histochemical analysis of the eggs of Pelodiscus sinesis. J. Anhui. Agric. Sci. 21, 232–44.Google Scholar
Han, X.K., Zhang, L., Hei, N.N. & Chen, Q.S. (2007). Sperm storage in male and female soft-shelled turtles, Trionyx sinensis in hibernation. Chi. J. Fishery Sci. 14, 706–11.Google Scholar
Han, X.K., Zhang, L., Li, M.Y., Bao, H.J., Hei, N.N. & Chen, Q.S. (2008). Seasonal changes of sperm storage and correlative structures in male and female soft-shelled turtles, Trionyx sinensis. Anim. Reprod. Sci. 108, 435–45.Google Scholar
Hernández-Franyutti, A., Uribe Aranzábal, M.C. & Guillette, L.J. Jr. (2005). Oogenesis in the viviparous matrotrophic lizard Mabuya brachypoda. J. Morphol. 265, 152–64.CrossRefGoogle ScholarPubMed
Huang, P.L., Pan, S.W. & Jiang, S.Y. (1999). Development and histological observation of the ovaries in Bungarus multicinctus Blyth before, during and after hibernation. J. Guang Xi Agric. Sci. 17, 90–4.Google Scholar
Iwabe, N., Hara, Y., Kumazawa, Y., Shibamoto, K., Saito, Y., Miyata, T. & Katoh, K. (2005). Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA–coded proteins. Mol. Biol. Evol. 22, 810–3.CrossRefGoogle Scholar
Goldberg, S.R. (1968). Seasonal ovarian histology of the ovoviviparous iguanid lizard Sceloporus jarrovi copes. J. Morphol. 132, 256–76.Google Scholar
Gómez, D. & Ramírez-Pinilla, M.P. (2004). Ovarian histology of the placentotrophic Mabuya mabouya (Squamata, Scincidae). J. Morphol. 259, 90–105.CrossRefGoogle ScholarPubMed
Guraya, S.S. (1989). Ovarian Follicles in Reptiles and Birds. Springer-Verlag, Berlin.CrossRefGoogle Scholar
Karen, A.B., Archie, C. & Anne, B.M. (1985). Reproductive biology of the hawksbill Eretmochelys imbricata at Tortuguero, Costa Rica, with notes on the ecology of the species in the Caribbean. Biol. Conserv. 34, 352–68.Google Scholar
Mari, C.A. & Guillette, L.J. (2000). Oogenesis and ovarian histology of the American alligator, Alligator mississippiensis. J. Morphol. 245, 225–40.Google Scholar
Marina, P., Maurizio, R., Loredana, R., Ermelinda, L. & Piero, A. (2002). An ultrastructural study on the vitellogenesis in the spotted ray Torpedo marmorata. Gen. Comp. Endocrinol. 128, 171–9.Google Scholar
Mordechai, A., Voiker, H., Shoshana, L. & Helene, T. (1984). The cellular envelope of oocytes in teleosts. Cell Tissue Res. 235, 403–10.Google Scholar
Mou, Z.B., Xu, G.F. & Yang, S.Y. (2008). Development and function of ovarian follicular cells in Brachymystax lenok. Chi. J. Fishery Sci. 15, 167–71.Google Scholar
Matsumoto, T., Yamano, K., Kitamura, M. & Hara, A. (2008). Ovarian follicle cells are the site of vitellogenin synthesis in the Pacific abalone Haliotis discus hannai. Comp. Biochem. Physiol. Part A 149, 293–8.CrossRefGoogle ScholarPubMed
Perry, M.M., Gilbert, A.B. & Evans, A.J. (1978). Electron microscope observations on the ovarian follicle of the domestic fowl during the rapid growth phase. J. Anat. 125, 481–97.Google ScholarPubMed
Rahil, K.S. & Narbaitz, R. (1973). Ultrastructural studies on the relationship between follicular cells and growing oocytes in the turtle Pseudemys scripta elegans. J. Anat. 115, 175–86.Google ScholarPubMed
Reston, S.B., Parameswaran, S., Lekha, D., Oommen, V.O. & Mohammad, A.A. (2007). Ultrastructural observations of previtellogenic ovarian follicles of the Caecilians Ichthyophis tricolor and Gegeneophis ramaswamii. J. Morphol. 268, 329–42.Google Scholar
Reston, S.B., Lekha, D., Mathew, S., Oommen, V.O. & Mohammed, A.A. (2008). Stages in follicle cell/oocyte interface during vitellogenesis in caecilians Ichthyophis tricolor and Gegeneophis ramaswamii: a transmission electron-microscopic study. Cell Tissue Res. 331, 519–28.Google Scholar
Rieppel, O. (1996). Testing homology by congruence: the pectoral girdle of turtles. Proc. R. Soc. Lond. B 263, 1395–8.Google ScholarPubMed
Rogers, S.W. (1999). Allosaurus, crocodiles and birds: evolutionary clues from spiral computed tomography of an endocast. Anat. Rec. (New Anat). 257, 162–73.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Saxena, R.C. (1979). Histochemical observation of the cortical zone of oocyte of Indian wall lizard, Hemidactylus flaviviridis (Rüppel). Folia Histochem. Cytochem. (Krakow) 17, 297–304.Google ScholarPubMed
Tadei, C. & Andreuccetti, P. (1990). Structural modifications of the nuclear components during lizard oogenesis in relation to differentiation of the follicular epithelium. Cell Differ. Dev. 29, 205–15.CrossRefGoogle Scholar
Tammaro, S., Andreuccetti, P., Filosa, S., Indolfi, P., Prisco, M. & Motta, C.M. (1998). Structural and functional modifications of the nucleolus during previtellogenic oocyte growth in the lizard Podarcis sicula. Mol. Reprod. Dev. 51, 413–20.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Wallace, R.A. & Selman, K. (1990). Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron Microsc. Tech. 16, 175–201.CrossRefGoogle ScholarPubMed
Yang, Z.C., Niu, C.J. & Sun, R.Y. (1999). The advancement of biological research in soft-shelled turtles, Trionyx sinensis. Chi. J. Zool. 34, 41–4.Google Scholar
Zhang, L., Han, X.K., Qi, Y.Y., Liu, Y. & Chen, Q.S. (2008). Seasonal effects on apoptosis and proliferation of germ cells in the testes of the Chinese soft-shelled turtle, Pelodiscus sinensis. Theriogenology 69, 1148–58.CrossRefGoogle ScholarPubMed
Zhou, K.Y. (2001). Molecular phylogenetics of amphibians and reptiles. Zool. Res. 5, 397–405.Google Scholar
Zhang, Y. (2001). Research progress on development and atresia in follicular and apoptosis in ovary. Fore. Medi. Sci. (Family Planning) 20, 194–8.Google Scholar
Zhang, Y.G., Yang, G.Z. & Jin, L. (2004). Studies on the developmental ultrastructure of follicle cell of ovary and egg envelope in Silurus meridionalis Chen. Chi. J. Southwest Normal Univ. (Nat. Sci.) 29, 1009–15.Google Scholar