Abstract
Hybrid water frogsRana esculenta reproduce by hybridogenesis: one parental genome (ofRana lessonae) is excluded in the germ line, the other (ofRana ridibunda) is clonally transmitted to haploid gametes. The two parental species differ in that the amount of centromeric heterochromatin revealed by differential staining is much higher inRana ridibunda. An abundant, tandemly arrayed, centromeric satellite DNA, designated RrS1, is revealed inRana ridibunda genomes by the restriction endonucleaseStul, which generates a major repetitive sequence fragment of 300 and a minor one of 200 bp. This AT-rich (68%) satellite family is located at the centromeres of the five largest chromosomes (1–5) and of a medium to small heterobrachial one (8 or 9); it thus constitutes only part of the centromeric heterochromatin that characterizes allRana ridibunda chromosomes. RrS1 represents about 2.5% of the genome ofRana ridibunda; it may represent as little as 0.2% of the genome ofRana lessonae, and cannot be detected inXenopus laevis frogs orSalamandra salamandra andTriturus carnifex salamanders. Segments of the satellite sequence are similar to sequences of yeast centromeric DNA element CDEIII and of the mammalian CENP-B box. A role for RrS1 and other centromeric satellite DNAs in the germ line genome exclusion of the hybridogenetic frog hybrids, although suggested, has not yet been demonstrated.
References
Baldwin L, Macgregor HC (1985) Centromeric satellite DNA in the newtTriturus cristatus karelinii and related species: its distribution and transcription on lampbrush chromosomes.Chromosoma 92: 100–107.
Beerli P, Hotz H, Tunner HG, Heppich S, Uzzell T (1994) Two new water frog species from the Aegean islands Crete and Karpathos (Amphibia, Salientia, Ranidae).Notulae Naturae, Acad Nat Sci Philadelphia 470: 1–9.
Borkin LJ, Vinogradov AE, Rosanov JM, Caune IA (1987) Hemiclonal inheritance in the hybridogenetic complexRana esculenta: evidence from flow DNA-cytometry.Dokl Akad Nauk SSSR 295: 1261–1264.
Bucci S, Ragghianti M, Mancino Get al. (1990) Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybridRana esculenta and its parental species.J Exp Zool 255: 37–56.
Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences with ESEE.Comp Appl Biosci 5: 233–234.
Clarke L (1990) Centromeres of budding and fission yeast.Trends Genet 6: 150–154.
Cremisi F, Vignali R, Batistoni R, Barsacchi G (1988) Heterochromatic DNA inTriturus (Amphibia, Urodela). II. A centromeric satellite DNA.Chromosoma 97: 204–211.
Goddard KA, Schultz RJ (1993) Aclonal reproduction by polyploid members of the clonal hybrid speciesPhoxinus eos-neogaeus (Cyprinidae).Copeia 1993: 650–660.
Graf J-D, Polls Pelaz M (1989) Evolutionary genetics of theRana esculenta complex. In: Dawley RM, Bogart JP, eds.Evolution and Ecology of Unisexual Vertebrates. Albany, NY: New York State Mus Bull 466, pp 289–302.
Günther R (1975) Untersuchungen der Meiose bei Männchen vonRana ridibunda Pall.,Rana lessonae Cam. und deren Bastardform ‘Rana esculenta’ L. (Anura).Biol Zentralbl 94: 277–294.
Günther R (1990)Die Wasserfrösche Europas (Anura — Froschlurche). Wittenberg Lutherstadt: Die Neue Brehm-Bücherei.
Heppich S, Tunner HG, Greilhuber J (1982) Premeiotic chromosome doubling after genome elimination during spermatogenesis of the species hybridRana esculenta.Theor Appl Genet 61: 101–104.
Hieter P, Pridmore D, Hegemann JH, Davis RW, Philippsen P (1985) Functional selection and analysis of yeast centromeric DNA.Cell 42: 913–921.
Hotz H, Uzzell T (1983) Interspecific hybrids ofRana ridibunda without germ line exclusion of a parental genome.Experientia 39: 538–540.
Hotz H, Mancino G, Bucci-Innocenti S, Berger L, Uzzell T (1985)Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecies hybrids.J Exp Zool 236: 199–210.
Macgregor HC, Sessions SK (1986) The biological significance of variation in satellite DNA and heterochromatin in newts of the genusTriturus: an evolutionary perspective.Phil Trans R Soc Lond B 312: 243–259.
Mancino G, Ragghianti M, Bucci-Innocenti S (1977) Cytotaxonomy and cytogenetics in European newt species. In: Taylor DH, Guttman SI, eds.The Reproductive Biology of Amphibians. New York: Plenum Press, pp 411–477.
Mantovani B, Scali V (1992) Hybridogenesis and androgenesis in the stick-insectBacillus rossius-grandii benazzii (Insecta, Phasmatodea).Evolution 46: 783–796.
Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite.J Cell Biol 109: 1963–1973.
Mazin AL, Borkin LJ (1979) Nuclear DNA content in green frogs of the genusRana.Mitt Zool Mus Berlin 55: 217–224.
Mezhzherin SV (1992) A new species of green frogsRana terentievi sp. nova (Amphibia, Ranidae) from South Tadjikistan.Dokl Akad Nauk Ukrainy 1992: 154–157.
Nardi I, Ragghianti M, Mancino G (1973) Banding patterns in newt chromosomes by the Giemsa staining.Chromosoma 40: 321–331.
Polls Pelaz M (1994) Natural ameiosis in unisexual all-male allotriploids ofRana kl.esculenta. PhD dissertation, Universitat de Barcelona.
Sanger F, Nicken S, Coulson AR (1977) DNA sequencing with chian-terminating inhibitors.Proc Natl Acad Sci USA 74: 5463–5467.
Schultz RJ (1969) Hybridization, unisexuality, and polyploidy in the teleostPoeciliopsis (Poeciliidae) and other vertebrates.Am Nat 103: 605–619.
Schultz RJ (1977) Evolution and ecology of unisexual fishes. In: Hecht MK, Steere WC, Wallace B, eds.Evoluutionary Biology, New York: Plenum Press, pp. 277–331.
Schwindinger WF, Warner JR (1984) DNA sequence analysis on the IBM-PC.Nucleic Acids Res 12: 601–604.
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis.J Mol Biol 98: 503–517.
Sugimoto K, Muro Y, Himeno M (1992) Anti-helix-loop-helix domain antibodies: discovery of autoantibodies that inhibit DNA binding activity of human centromere protein B (CENP-B).J Biochem 111: 478–483.
Sugimoto K, Furukawa K, Himeno M (1994) Functional cloning of centromere protein B (CENP-B) box-enriched alphoid DNA repeats utilizing the sequence-specific DNA binding activity of human CENP-Bin vitro.Chrom Res 2: 453–459.
Tautz D, Renz M (1983) An optimized freeze-squeeze method for the recovery of DNA fragments from agarose gels.Anal Biochem 132: 14–19.
Tunner HG (1974) Die klonale Struktur einer Wasserfrosch-population.Z Zool Syst Evolforsch 12: 309–314.
Tunner HG, Heppich S (1981) Premeiotic genome exclusion during oogenesis in the common edible frog,Rana esculenta.Naturwissenschaften 68: 207–208.
Tunner HG, Heppich-Tunner S (1991) Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog.Naturwissenschaften 78: 32–34.
Vinogradov AE, Rozanov JM, Caune IA, Borkin LJ (1988) Genome elimination of one of the parents in the hybridogenic speciesRana esculenta prior to premeiotic DNA synthesis.Citologija 30: 691–698.
Vinogradov AE, Borkin LJ, Günther R, Rosanov JM (1990) Genome elimination in diploid and triploidRana esculenta males: cytological evidence from DNA flow cytometry.Genome 33: 619–627.
Vinogradov AE, Borkin LJ, Günther R, Rosanov JM (1991) Two germ cell lineages with genomes of different species in one and the same animal.Hereditas 114: 245–251.
Vinogradov AE, Borkin LJ (1993) Allometry of base pair specific-DNA contents in Tetrapoda.Hereditas 118: 155–163.
Willard HF (1990) Centromeres of mammalian chromosomes.Trends Genet 6: 410–416.
Willard HF (1992) Centromeres — primary constrictions are primarily complicated.Hum Mol Genet 1: 667–668.
Willard HF, Waye JS (1987) Hierarchical order in chromosome-specific human alpha satellite DNA.Trends Genet 3: 192–198.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ragghianti, M., Guerrini, F., Bucci, S. et al. Molecular characterization of a centromeric satellite DNA in the hemiclonal hybrid frogRana esculenta and its parental species. Chromosome Res 3, 497–506 (1995). https://doi.org/10.1007/BF00713965
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00713965