Abstract
Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) was examined using conventional cytogenetic and molecular techniques. Variation was observed in the number, size and position of rDNA loci on the sex pair. Fluorescence in situ hybridization (FISH) analyses showed that the sex chromosomes of Arctic char lack the repetitive DNA sequences (MboI/BglII family) that are a prominent feature of the sex chromosomes of lake trout (S. namaycush). Southern analyses of genomic DNAs using an rDNA fragment as probe revealed extensive restriction fragment length polymorphism (RFLP) variation among individuals. Despite the presence of variation in all aspects of this rDNA locus, no sex-specific differences were detected. Repetitive DNAs (multicopy rDNA as in Arctic char or tandem repetitive DNA as in lake trout) appear to play important but different roles in the evolution of the sex chromosomes in these species.
Similar content being viewed by others
References
Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner JB, ed. Evolutionary Genetics of Fishes. New York: Plenum Publishing, pp 1–53.
Charlesworth B (1991) The evolution of sex chromosomes. Science 251: 1030–1033.
Charlesworth B, Langley CH, Stephan W (1986) The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics 112: 947–962.
Devlin RH, McNeil BK, Groves TDD, Donaldson EM (1991) Isolation of a Y-chromosomal DNA probe capable of determining genetic sex in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 48: 1606–1612.
Donaldson EM (1986) The integrated development and application of controlled reproduction techniques in Pacific salmonid aquaculture. Fish Physiol Biochem 2: 9–24.
Foresti F, Almeida Toledo LF, Toledo FSA (1981) Polymorphic nature of nucleolus organizer regions in fishes. Cytogenet Cell Genet 31: 137–144.
Frolov SV (1995) Comparative karyology and karyotype evolution of chars. J Ichthyol 35: 14–23.
Gold JR (1979) Cytogenetics. In: Hoar WS, Randall DJ, Brett JR, eds. Fish Physiology. Vol. VIII. New York: Academic Press, pp 353–405.
Green DM (1988) Heteromorphic sex chromosomes in the rare and primitive frog Leiopelma hamiltoni from New Zealand. J Hered 79: 165–169.
Hartley SE, Davidson WS (1994) Characterization and distribution of genomic repeat sequences from Arctic char (Salvelinus alpinus). In Beaumont AR (ed), Genetics and Evolution of Aquatic Organisms. London: Chapman & Hall, pp 271–280.
Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36: 1014–1015.
Lockwood SF, Derr JN (1992) Intra-and interspecific genome-size variation in the Salmonidae. Cytogenet Cell Genet 59: 303–306.
May B, Johnson KR, Wright JE, Jr (1989) Sex linkage in salmonids: evidence from a hybridized genome of brook trout and Arctic charr. Biochem Genet 27: 291–301.
Muller HJ (1964) The relation of recombination to mutational advance. Mut Res 43: 165–229.
Nakayama I, Foresti F, Tewari R, Schartl, Chourrout D (1994) Sex chromosome polymorphism and heterogametic males revealed by two cloned DNA probes in the ZW/ZZ fish Leporinus elongatus. Chromosoma 103: 31–39.
Nanda I, Feichtinger W, Schmid M, Schrö der JH, Zischler H, Epplen JT (1990) Simple repetitive sequences are associated with differentiation of the sex chromosomes in the guppy fish. J Mol Evol 30: 456–462.
Nanda I, Schartl M, Epplen JT, Feichtinger W, Schmid M (1993) Primitive sex chromosomes in Poeciliid fishes harbor simple repetitive DNA sequences. J Exp Zool 265: 301–308.
Orr HA (1990) 'Why polyploidy is rarer in animals than in plants’ revisited. Am Nat 136: 759–770.
Pendas AM, Moran P, Garcia-Vazquez E (1993a) Ribosomal RNA genes are interspersed throughout a heterochromatic chromosome arm in Atlantic salmon. Cytogenet Cell Genet 63: 128–130.
Pendas AM, Moran P, Garcia-Vazquez E (1993b) Multi-chromosomal location of ribosomal RNA genes and hetero-chromatic association in brown trout. Chrom Res 1: 63–67.
Phillips RB, Ihssen PE (1985) Identification of sex chromosomes in lake trout (Salvelinus namaycushit). Cytogenet Cell Genet 39: 14–18.
Phillips RB, Reed KM (1996) Application of fluorescence in situ hybridization (FISH) techniques to fish genetics: A review. Aquaculture 140: 197–216.
Phillips RB, Pleyte KA, Hartley SE (1988) Stock-specific differences in the number and chromosome positions of the nucleolar organizer regions in Arctic char (Salvelinus alpinus). Cytogenet Cell Genet 48: 9–12.
Phillips RB, Pleyte KA, Ihssen PE (1989a) Patterns of chromosomal nucleolar organizer region (NOR) variation in fishes of the genus Salvelinus. Copeia 1989: 47–53.
Phillips RB, Pleyte KA, Van Ert LM, Hartley SE (1989b) Evolution of nucleolar organizer regions and ribosomal RNA genes in Salvelinus. Physiol Ecol Japan 1: 429–447.
Phillips RB, Zajicek KD, Ihssen PE (1989c) Population differences in chromosome-banding polymorphisms in lake trout. Trans Am Fish Soc 118: 64–73.
Phillips RB, Pleyte KA, Brown MR (1992) Salmonid phylogeny inferred from ribosomal DNA restriction maps. Can J Fish Aquat Sci 49: 2345–2353.
Rab P, Reed KM, Ponce de Leon A, Phillips RB (1996) A new method for detecting nucleolus organizer regions in fish chromosomes using denaturation and propidium iodine staining. Biotech Histochem 71: 157–162.
Reed KM, Phillips RB (1995a) Molecular characterization and cytogenetic analysis of highly repetitive DNAs of lake trout, Salvelinus namaycush. Chromosoma 104: 242–251.
Reed KM, Phillips RB (1995b) Molecular cytogenetic analysis of the double-CMA3 chromosome of lake trout, Salvelinus namaycush. Cytogenet Cell Genet 70: 104–107.
Reed KM, Bohlander SK, Phillips RB (1995) Microdissection of the Y chromosome and fluorescence in situ hybridization analysis of the sex chromosomes of lake trout, Salvelinus namaycush. Chrom Res 3: 221–226.
Reed KM, Oakley TH, Phillips RB (1997) An AluI repetitive element isolated from lake trout (Salvelinus namaycush), maps to the intergenic spacer region of the rDNA cistron. Gene 186: 7–11.
Schmid M, Haaf T, Geile B, Sims S (1983) Chromosome banding in Amphibia: VII. An unusual XY/XX sex chromosome system in Gastrotheca riobambae (Anura, Hylidae). Chromosoma 88: 69–82.
Thorgaard GH (1977) Heteromorphic sex chromosomes in male rainbow trout. Science 196: 900.
Zhuo L, Reed KM, Phillips RB (1995) Hypervariability of ribosomal DNA at multiple chromosomal sites in lake trout (Salvelinus namaycush). Genome 38: 487–496.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Reed, K.M., Phillips, R.B. Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related. Chromosome Res 5, 221–227 (1997). https://doi.org/10.1023/A:1018411417816
Issue Date:
DOI: https://doi.org/10.1023/A:1018411417816