[en] Two types of nucleolus can be distinguished among eukaryotic cells: a tri-compartmentalized nucleolus in amniotes and a bi-compartmentalized nucleolus in all the others. However, though the nucleolus' ultrastructure is well characterized in mammals and birds, it has been so far much less studied in reptiles. In this work, we examined the ultrastructural organization of the nucleolus in various tissues from different reptilian species (three turtles, three lizards, two crocodiles, and three snakes). Using cytochemical and immunocytological methods, we showed that in reptiles both types of nucleolus are present: a bi-compartmentalized nucleolus in turtles and a tri-compartmentalized nucleolus in the other species examined in this study. Furthermore, in a given species, the same type of nucleolus is present in all the tissues, however, the importance and the repartition of those nucleolar components could vary from one tissue to another. We also reveal that, contrary to the mammalian nucleolus, the reptilian fibrillar centers contain small clumps of condensed chromatin and that their surrounding dense fibrillar component is thicker. Finally, we also report that Cajal bodies are detected in reptiles. Altogether, we believe that these results have profound evolutionarily implications since they indicate that the point of transition between bipartite and tripartite nucleoli lies at the emergence of the amniotes within the class Reptilia.
Alibardi L. Differentiation of snake epidermis, with emphasis on the shedding layer. J. Morphol. 2005, 264:178-190.
Alibardi L., Thompson M.B. Epidermal differentiation during carapace and plastron formation in the embryonic turtle Emydura macquarii. J. Anat. 1999, 194:531-545.
Alibardi L., Thompson M.B. Fine structure of the developing epidermis in the embryo of the American alligator (Alligator mississippiensis, Crocodilia, Reptilia). J. Anat. 2001, 198:265-282.
Alibardi L., Thompson M.B. Epidermal differentiation during ontogeny and after hatching in the snake Liasis fuscus (Pythonidae, Serpentes, Reptilia), with emphasis on the formation of the shedding complex. J. Morphol. 2003, 256:29-41.
Alibardi L., Maurigii M.G., Taddei C. Immunocytochemical and eletrophoretic distribution of cytokeratins in the regenerating epidermis of the lizard Podarcis muralis. J. Morphol. 2000, 246:179-191.
Boisvert F.M., van Koningsbruggen S., Navascués J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
Bogolyubov D., Parfenov V. Structure of the insect oocyte nucleus with special reference to interchromatin granule clusters and cajal bodies. Int. Rev. Cell Mol. Biol. 2008, 269:59-110.
Cheutin T., O'Donohue M.-F., Beorchia A., Vandelaer M., Kaplan H., Deféver B., Ploton D., Thiry M. Three-dimensional organization of active rRNA genes within the nucleolus. J. Cell Sci. 2002, 115:3297-3307.
Cioce M., Lamond A.I. Cajal bodies: a long history of discovery. Ann. Rev. Cell Dev. Biol. 2005, 21:105-131.
Derenzini M., Pasquinelli G., O'Donohue M.-F., Ploton D., Thiry M. Structural and functional organization of ribosomal genes within the mammalian cell nucleolus. J. Histochem. Cytochem. 2006, 54:131-145.
Faure J., Mesure M., Tort M., Dufaure J.-P. Polyploidization and other nuclear changes during the annual cycle of an androgen-dependant organ, the liard epididymis. Biol. Cell 1987, 60:193-208.
Hadjiolov A.A. The Nucleolus and Ribosome Biogenesis 1985, Springer-Verlag, Wien, New-York, pp. 1-268.
Hernandez-Verdun D., Roussel P., Thiry M., Sirri V., Lafontaine D. The nucleolus: structure/function relationship in RNA metabolism. Willey Interdisciplinary Reviews: RNA. 2010, 1:415-431.
Hill R.V. Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. Syst. Biol. 2005, 54:530-547.
Hubert M.J. Preliminary data on " fibrillary centers" of the nucleolus of various cells of the ovarian follicle of a lizard Lacerta muralis Laur. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 1975, 281:271-273.
Iwabe N., Hara Y., Kumazawa Y., Shibamoto K., Saito Y., Miyata T., Katoh K. Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol. Biol. Evol. 2005, 22:810-813.
Jennane A., Thiry M., Goessens G. Identification of coiled body-like structures in meristematic cells of Pisum sativum cotyledonary buds. Chromosoma 1999, 108:132-142.
Lee M.S.Y. Molecules, morphology, and the monophyly of diapsid reptiles. Contrib. Zool. 2001, 70:1-22.
Mallatt J., Winchell C.J. Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star. Mol. Phylogenet. Evol. 2007, 43:1005-1022.
Morris G.E. The Cajal body. Biochim. Biophys. Acta 2008, 1783:2108-2115.
Olson M.O.J. Nontraditional roles of the nucleolus. The Nucleolus 2004, 329-342. Landes: Biosciences/eurekah.com, Austin. M.O.J. Oson (Ed.).
Ploton D., Menager M., Adnet J.J. Simultaneous high resolution localization of Ag-NOR proteins and nucleoproteins in interphasic and mitotic nuclei. Histochem. J. 1984, 16:897-906.
Rieppel O., Reisz R.R. The origin and early evolution of turtles. Ann. Rev. Ecol. Syst. 1999, 30:1-22.
Romer A.S. Vertebrate Paleontology 1996, University of Chicago. third ed.
Roth J., Bendayan M., Carlemalm E., Villiger W., Garavito M. Enhancement of structural preservation and immunocytochemical staining in low temperature embedded pancreatic tissue. J. Histochem. Cytochem. 1981, 29:663-671.
Sirri V., Urcuqui-Inchima S., Roussel P., Hernandez-Verdun D. Nucleolus: the fascinating nuclear body. Histochem. Cell Biol. 2008, 129:13-31.
Thiry M. Highly sensitive immunodetection of DNA on sections with exogenous terminal deoxynucleotidyl transferase and non-isotopic nucleotide analogues. J. Histochem. Cytochem. 1992, 40:411-419.
Thiry M., Cheutin T., Lamaye F., Thelen N., Meier U.T., O'Donohue M.-F., Ploton D. Localization of Nopp140 within mammalian cells during interphase and mitosis. Histochem. Cell Biol. 2009, 132:129-140.
Thiry M., Cheutin T., O'Donohue M.-F., Kaplan H., Ploton D. Dynamics and three-dimensional localization of ribosomal RNA within the nucleolus. RNA 2000, 6:1750-1761.
Thiry M., Goessens G. The Nucleolus During Cell Cycle 1996, R.G. Landes Company, Chapman and Hall, New-York, pp. 1-144.
Thiry M., Lafontaine D.L. Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 2005, 15:194-199.
Thiry M., Lepoint A., Goessens G. Re-evaluation of the site of transcription in Ehrlich tumour cell nucleoli. Biol. Cell 1985, 54:57-64.
Thiry M., Schoonbroodt S., Goessens G. Cytochemical distinction of various nucleolar components in insect cells. Biol. Cell 1991, 72:133-140.
Verheggen C., Mouaikel J., Thiry M., Blanchard J.M., Tollervey D., Bordonné R., Lafontaine D.L., Bertrand E. Box C/D small nucleolar RNA trafficking involves small nucleolar RNP proteins, nucleolar factors and a novel nuclear domain. EMBO J. 2000, 20:5480-5490.
Wassef M., Burglen J., Bernhard W. A new method for visualization of preribosomal granules in the nucleolus after acetylation. Biol. Cell 1979, 34:153-158.
Weibel E.R. Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 1969, 26:235-302.
Werneburg I., Sánchez-Villagra M.R. Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evol. Biol. 2009, 9:82.
Willinston S.W. The phylogeny and classification of reptiles. J. Geol. 1917, 25:411-421.
Zardoya R., Meyer A. The evolutionary position of turtles revised. Naturwissenschaften 2001, 88:193-200.
