Abstract
The mitotic and meiotic chromosomes of the marsupial frog Gastrotheca riobambae were analysed with various banding techniques. The karyotype of this species is distinguished by considerable amounts of constitutive heterochromatin and unusual, heteromorphic XY sex chromosomes. The Y chromosome is considerably larger than the X chromosome and almost completely heterochromatic. The analysis of the banding patterns obtained with GC- and AT-base-pair-specific fluorochromes shows that the constitutive heterochromatin in the Y chromosome consists of at least three different structural categories. The only nucleolus organizer region (NOR) of the karyotype is localized in the short arm of the X chromosome. This causes a sex-specific difference in the number of NOR: female animals have two NORs in diploid cells, male animals one. No cytological indications were found for the inactivation of one of the two X chromosomes in the female cells. In male meiosis, the heteromorphic sex chromosomes form a characteristic sex-bivalent by pairing their telomeres in an end-to-end arrangement. The significance of the XY/XX sex chromosomes of G. riobambae for the study of X-linked genes in Amphibia, the evolution of sex chromosomes and their specific DNA sequences, and the significance of the meiotic process of sex chromosomes are discussed.
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Barr HJ, Ellison JR (1972) Ectopic pairing of chromosome regions containing chemically similar DNA. Chromosoma 39:53–61
Barr HJ, Esper H (1963) Nucleolar size in cells of Xenopus laevis in relation to nucleolar competition. Exp Cell Res 31:211–214
Beçak W, Beçak ML, Nazareth HRS, Ohno S (1964) Close karyological kinship between the reptilian suborder Serpentes and the class Aves. Chromosoma 15:606–617
Birnstiel, ML, Wallace H, Sirlin JL, Fischberg M (1966) Localization of the ribosomal DNA complements in the nucleolus organizer region of Xenopus laevis. In: (Vincent WS, Miller OL, eds) International symposium on the nucleolus. Its structure and function. NCI Monograph 23. Bethesda: Natl Cancer Inst, pp. 431–448
Buys CHCM, Osinga J (1980) Abundance of protein-bound sulfhydril and disulfide groups at chromosomal nucleolus organizing regions — a cytochemical study on the selective silver staining of NORs. Chromosoma 77:1–11
Chen TR, Ebeling AW (1968) Karyological evidence of female heterogamety in the mosquito fish Gambusia affinis (Baird and Girard). Copeia 1:70–75
Chromosome atlas (1971–1975) Fish, amphibians, reptiles and birds (Benirschke K, Hsu TC, eds), folios Nos. R-17, R-31, R-37 and R-38. Springer, New York-Heidelberg-Berlin
Duellman WE (1974) A systematic review of the marsupial frogs (Hylidae: Gastrotheca) of the Andes of Ecuador. Occas. Papers Mus. Nat. Hist. Univ. Kansas 22:1–27
Duellman WE (1977) Liste der rezenten Amphibien und Reptilien. Hylidae, Centrolenidae, Pseudidae. In: (Mertens R, Hennig W, eds) Das Tierreich 95. Walter de Gruyter, Berlin-New York pp. 12–21
Duellman WE, Fritts TH (1972) A taxonomic review of the southern Andean marsupial frogs (Hylidae: Gastrotheca). Occas. Papers Mus. Natl. Hist. Univ. Kansas 9:1–37
Engel W, Zenzes MT, Schmid M (1977) Activation of mouse ribosomal RNA genes at the 2-cell stage. Hum. Genet. 38:57–63
Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50
Hayman DL, Rofe R (1977) Marsupial sex chromosomes. In: (Calaby JH, Tyndale-Biscoe CH, eds) Reproduction and evolution. Australian Academy of Science, Canberra pp. 69–79
Hayman D, Sharp P (1981) Hoechst 33258 induced uncondensed sites in marsupial chromosomes. Chromosoma 83:249–262
Hayman DL, Ashworth LK, Carrano AV (1982) The relative DNA contents of the eutherian and marsupial X chromosomes. Cytogenet. Cell Genet. 34:265–270
Howell WM (1977) Visualization of ribosomal gene activity: silver stains proteins associated with rRNA transcribed from oocyte chromosomes. Chromosoma 62:361–367
Hsu TC, Cooper JEK, Mace ML, Brinkley BR (1971) Arrangement of centromeres in mouse cells. Chromosoma 34:73–87
Hsu TC, Spirito SE, Pardue ML (1975) Distribution of 18 + 28S ribosomal genes in mammalian genomes. Chromosoma 53:25–36
Iturra P, Veloso A (1981) Evidence for heteromorphic sex chromosomes in male amphibians (Anura: Leptodactylidae). Cytogenet. Cell Genet. 31:108–110
Jalal SM, Clark RW, Hsu TC, Pathak S (1974) Cytological differentiation of constitutive heterochromatin. Chromosoma 48:391–403
Jones KW, Singh L (1981) Conserved repeated DNA sequences in vertebrate sex chromosomes. Hum. Genet. 58:46–53
Kahn J (1962) The nucleolar organizer in the mitotic chromosome complement of Xenopus laevis. Quart. J. Micr. Sci. 103:407–409
Kurnit DM (1979) Satellite DNA and heterochromatin variants: the case for unequal mitotic crossing over. Hum. Genet. 47:169–186
Lin MS, Comings DE, Alfi OS (1977) Optical studies of the interaction of 4′-6-diamidino-2-phenylindole with DNA and metaphase chromosomes. Chromosoma 60:15–25
Miller L, Knowland J (1970) Reduction of ribosomal RNA synthesis and ribosomal RNA genes in a mutant of Xenopus laevis which organizes only a partial nucleolus. II. The number of ribosomal RNA genes in animals of different nucleolar types. J. Molec. Biol. 53:329–338
Miller DA, Dev VG, Tantravahi R, Miller OJ (1976a) Suppression of human nucleolus organizer activity in mouse-human somatic hybrid cells. Exp Cell Res 101:235–243
Miller OJ, Miller DA, Dev VG, Tantravahi R, Croce CM (1976b) Expression of human and suppression of mouse nucleolus organizer activity in mouse-human somatic cell hybrids. Proc Natl Acad Sci 73:4531–4535
Morescalchi A (1971) Comparative karyology of the Amphibia. Boll Zool 38:317–320
Morescalchi A (1973) Amphibia. In: (Chiarelli AB, Capanna E, eds) Cytotaxonomy and vertebrate evolution. Academic Press, London-New York pp. 233–348
Noble GK (1931) The biology of the Amphibia. McGraw-Hill Book New York
Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, Berlin-Heidelberg-New York
Rae PMM, Franke WW (1972) The interphase distribution of satellite DNA-containing heterochromatin in mouse nuclei. Chromosome 39:443–456
Ray-Chaudhuri SP, Singh L, Sharma T (1971) Evolution of sex chromosomes and formation of W chromatin in snakes. Chromosoma 33:239–251
Scanlan BE, Maxson LR, Duellman WE (1980) Albumin evolution in marsupial frogs (Hylidae: Gastrotheca). Evolution 34:222–229
Schempp W, Schmid M (1981) Chromosome banding in Amphibia. VI. BrdU-replication patterns in Anura and demonstration of XX/XY sex chromosomes in Rana esculenta. Chromosoma 83:697–710
Schmid M (1978a) Chromosome banding in Amphibia. I. Constitutive heterochromatin and nucleolus organizer regions in Bufo and Hyla. Chromosoma 66:361–388
Schmid M (1978b) Chromosome banding in Amphibia. II. Constitutive heterochromatin and nucleolus organizer regions in Ranidae, Microhylidae and Rhacophoridae. Chromosoma 68:131–148
Schmid M (1980a) Chromosome banding in Amphibia. V. Highly differentiated ZW/ZZ sex chromosomes and exceptional genome size in Pyxicephalus adspersus (Anura, Ranidae). Chromosoma 80:69–96
Schmid M (1980b) Chromosome banding in Amphibia. IV. Differentiation of GC- and AT-rich chromosome regions in Anura. Chromosoma 77:83–103
Schmid M (1980c) Chromosome evolution in Amphibia. In: (Müller H, ed) Cytogenetics of vertebrates. Birkhäuser, Basel-Boston-Stuttgart pp. 4–27
Schmid M (1983a) Chromosome banding in Amphibia. VII. Analysis of the structure and variability of NORs in Anura. Chromosoma 87:327–344
Schmid M (1983b) Evolution of sex chromosomes and heterogametic systems in Amphibia. Differentiation 23 (Suppl.): S 13–22
Schmid M, Vogel W, Krone W (1975) Attraction between centric heterochromatin in human chromosomes. Cytogenet. Cell Genet. 15:66–80
Schmid M, Olert J, Klett C (1979) Chromosome banding in Amphibia. III. Sex chromosomes in Triturus. Chromosoma 71:29–55
Schmid M, Löser C, Schmidtke J, Engel W (1982) Evolutionary conservation of a common pattern of activity of nucleolus organizers during spermatogenesis in vertebrates. Chromosoma 86:149–179
Schnedl W, Breitenbach M, Mikelsaar A-V, Stranzinger G (1977) Mithramycin and DIPI: a pair of fluorochromes specific for GC- and AT-rich DNA respectively. Hum Genet 36:299–305
Schweizer D (1976) Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58:307–324
Schweizer D (1981) Counterstain-enhanced chromosome banding. Hum Genet 57:1–14
Schweizer D, Ambros P, Andrle M (1978) Modification of DAPI banding on human chromosomes by prestaining with a DNA binding oligipeptide antibiotic, distamycin A. Exp Cell Res 111:327–332
Sessions SK (1980) Evidence for a highly differentiated sex chromosome heteromorphism in the salamander Necturus maculosus (Rafinesque). Chromosoma 77:157–168
Singh L, Purdom IF, Jones KW (1976) Satellite DNA and evolution of sex chromosomes. Chromosoma 59:43–62
Singh L, Purdom IF, Jones KW (1979) Human chromosomes contain repeated sequences related to sex chromosome associated DNA in snakes, birds, and insects. Cytogenet Cell Genet 25:204
Singh L, Purdom IF, Jones KW (1980) Sex chromosome associated satellite DNA: evolution and conservation. Chromosoma 79:137–157
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306
Thiébaud CH (1979a) The intra-nucleolar localization of amplified rDNA in Xenopus laevis oocytes. Chromosoma 73:29–36
Thiébaud CH (1979b) Quantitative determination of amplified rDNA and its distribution during oogenesis in Xenopus laevis. Chromosoma 73:37–44
Weisblum B (1973) Fluorescent probes of chromosomal DNA structure: three classes of acridines. Cold Spring Harb Symp Quant Biol 38:441–449
Weisblum B, de Haseth PL (1972) Quinacrine, a chromosome stain specific for deoxyadenylate-deoxythymidylate-rich regions in DNA. Proc Natl Acad Sci 69:629–632
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Schmid, M., Haaf, T., Geile, B. et al. Chromosome banding in Amphibia. Chromosoma 88, 69–82 (1983). https://doi.org/10.1007/BF00329505
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DOI: https://doi.org/10.1007/BF00329505