Advertisement

Chromosome Research

, Volume 11, Issue 4, pp 305–317 | Cite as

Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus)

  • Laura M. Daniels
  • Mary E. Delany
Article

Abstract

The 5S ribosomal (r) RNA genes encode a small (∼120-bp) highly-conserved component of the large ribosomal subunit. The objective of the present research was to study the molecular and cytogenetic organization of the chicken 5S rDNA. A predominant 2.2-kb gene (5Sα) consisting of a coding and intergenic spacer (IGS) region was identified in ten research and commercial populations. A variant gene repeat of 0.6 kb (5Sβ) was observed in some of the populations. Genetic linkage analysis and cytogenetic localization by fluorescence in-situ hybridization assigned the 5S rDNA to chromosome 9. The 5S rDNA array was determined to be 80.2 ± 7.0 kb upon electrophoretic sizing following EcoRV digestion. Sequence analysis of 5Sα IGS regions revealed considerable conservation between chicken subspecies (98.4% identity) as well as homology with vertebrate Pol III promoter and regulatory sequence motifs. Minor intraindividual sequence variation within 1000 bp of IGS was observed in four cloned Red Jungle Fowl (Gallus gallus gallus) 5Sα repeats (95.5% identity in this region). Sequence comparisons between IGS regions of 5Sα and 5Sβ genes indicated two short continuous (>20 bp) and many short non-continuous homologous regions as well as other conserved features such as promoter and termination motifs.

chicken fluorescence in-situ hybridization Gallus linkage 5S rRNA 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison D, Hall B (1985) Effects of alterations in the 3′ flanking sequence on in vivo and in vitro expression of the yeast SUP4-o tRNA Tyr gene. EMBO J 4: 2657-2664.Google Scholar
  2. Artavanis-Tsakonas S, Schedl P, Tschudi C et al. (1977) The 5S genes of Drosophila melanogaster. Cell 12: 1057-1067.Google Scholar
  3. Azad A, Failla P, Hanna P (1998) Inhibition of ribosomal subunit association and protein synthesis by oligonucliotides corresponding to defined regions of 18S rRNA and 5S rRNA. Biochem Biophys Res Commun 248: 51-56.Google Scholar
  4. Ban N, Nissen P, Hansen J, Moore P, Steitz T (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-919.Google Scholar
  5. Boulikas T (1993) Nature of DNA sequences at the attachment regions of genes to the nuclear matrix. J Cell Biochem 52: 14-22.Google Scholar
  6. Browder LW, Erickson CA, Jeffery WR (1991) Developmental Biology. San Francisco: Saunders College Publishing.Google Scholar
  7. Brown DD (1994) Some genes were isolated and their structure studied before the recombinant DNA era. BioEssays 16: 139-143.Google Scholar
  8. Brownlee G, Cartwright E (1975) The nucleotide sequence of the 5S RNA of chicken embryo fibroblasts. Nucleic Acids Res 2: 2279-2288.Google Scholar
  9. Carroll D, Brown D (1976) Repeating units of Xenopus laevis oocyte-type 5S DNA are heterogeneous in length. Cell 7: 467-475.Google Scholar
  10. Cloix C, Tutois S, Mathieu O et al. (2000) Analysis of 5S rDNA arrays in Arabidopsis thaliana: physical mapping and chromosome-specific polymorphisms. Genome Res 10: 679-690.Google Scholar
  11. Crittenden L, Provencher L, Santangelo I et al. (1993) Characterization of a Red Jungle Fowl by White Leghorn backcross reference population for molecular mapping of the chicken genome. Poult Sci 72: 334-348.Google Scholar
  12. Cronn R, Zhao X, Paterson A, Wendel J (1996) Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. J Mol Evol 42: 685-705.Google Scholar
  13. de la Serna I, Cujec T, Shi Y, Tyler B (2000) Non-coordinate regulation of 5S rRNA genes and the gene encoding the 5S rRNA-binding ribosomal protein homolog in Neurospora crassa. Mol Gen Genet 263: 987-994.Google Scholar
  14. Delany ME, Krupkin AB (1999) Molecular characterization of ribosomal gene variation within and among NORs segregating in specialized populations of chicken. Genome 42: 60-71.Google Scholar
  15. Delany ME, Muscarella DE, Bloom SE (1991) Formation of nucleolar polymorphisms in trisomic chickens and subsequent microevolution of rRNA gene clusters in diploids. J Hered 82: 213-220.Google Scholar
  16. Delany ME, Emsley A, Smiley M, Putnam JR, Bloom SE (1994) Nucleolar size polymorphisms in commercial layer chickens: determination of incidence, inheritance, and nucleolar sizes. Poult Sci 73: 1211-1217.Google Scholar
  17. Dinman J, Wickner R (1995) 5S rRNA is involved in fidelity of translational reading frame. Genetics 141: 95-105.Google Scholar
  18. Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299: 111-117.Google Scholar
  19. Drouin G (2000) Expressed retrotransposed 5S rRNA genes in the mouse and rat genomes. Genome 43: 213-215.Google Scholar
  20. Fedoroff NV, Brown DD (1978) The nucleotide sequence of oocyte 5S DNA in Xenopus laevis. I. The AT-rich spacer. Cell 13: 701-716.Google Scholar
  21. Fillon V, Morisson M, Zoorob R et al. (1998) Identification of 16 chicken microchromosomes by molecular markers using two-colour fluorescence in situ hybridization (FISH). Chromosome Res 6: 307-313.Google Scholar
  22. Ford P, Brown R (1976) Sequences of 5S ribosomal RNA from Xenopus mulleri and the evolution of 5S gene-coding sequences. Cell 8: 485-493.Google Scholar
  23. Frederiksen S, Cai H, Lomholt B, Levan G, Hallenberg C (1997) The rat 5S rRNA bona fide gene repeat maps to chromosome 19q12 → qter and the pseudogene repeat maps to 12q12. Cytogenet Cell Genet 76: 101-106.Google Scholar
  24. Geiduschek E, Kassavetis G (1992) RNA polymerase III transcription complexes. In: McKnight SL, Yamamoto KR, eds. Transcriptional Regulation. Cold Spring Harbour: Cold Spring Harbor Laboratory Press, pp 247-280.Google Scholar
  25. Groenen M, Cheng H, Bumstead N et al. (2000) A consensus linkage map of the chicken genome. Genome Res 10: 137-147.Google Scholar
  26. Gunnery S, Ma Y, Mathews M (1999) Termination sequence requirements vary among genes transcribed by RNA polymerase III. J Mol Biol 286: 745-757.Google Scholar
  27. Hallenberg C, Nielsen J, Frederiksen S (1994) Characterization of 5S genes from mouse. Gene 142: 291-295.Google Scholar
  28. Hart R, Folk W (1982) Structure and organization of a mammalian 5S gene cluster. J Biol Chem 257: 11706-11711.Google Scholar
  29. Hilder V, Dawson G, Vlad M (1983) Ribosomal 5S genes in relation to C-value in amphibians. Nucleic Acids Res 11: 2381-2390.Google Scholar
  30. Inafuku J, Nabeyama M, Kikuma Y et al. (2000) Chromosomal location and nucleotide sequences of 5S ribosomal DNA of two cyprinid species (Osteichthyes, Pisces). Chromosome Res 8: 193-199.Google Scholar
  31. Insua A, Freire R, Ríos J, Méndez J (2001) The 5S rDNA of mussels Mytilus galloprovincialis and M. edulis: sequence variation and chromosomal location. Chromosome Res 9: 495-505.Google Scholar
  32. Jeffreys A, Barber R, Bois P et al. (1999) Human minisatellites, repeat DNA instability and meiotic recombination. Electrophoresis 20: 1665-1675.Google Scholar
  33. Keith G, Nys Y, Fix C, Heyman T (1986) Accumulation and specific cleavage of 5S RNA in the isthmus of laying hen oviduct. Evidence for three chicken 5S RNA. Biochem Biophys Res Commun 138: 1405-1410.Google Scholar
  34. Kellogg E, Appels R (1995) Intraspecific and interspecific variation in 5S RNA genes are decoupled in diploid wheat relatives. Genetics 140: 325-343.Google Scholar
  35. Khaitovich P, Mankin AS (1999) Effect of antibiotics on large ribosomal subunit assembly reveals possible function of 5S rRNA. J Mol Biol 291: 1025-1034.Google Scholar
  36. Komiya H, Hasegawa M, Takemura S (1986) Differentiation of oocyte and somatic-type 5S rRNAs in animals. J Biochem 100: 369-374.Google Scholar
  37. Korn L, Brown D (1978) Nucleotide sequence of Xenopus borealis oocyte 5S DNA: comparison of sequences that flank several related eucaryotic genes. Cell 15: 1145-1156.Google Scholar
  38. Kost M, Alimov A, Sarafanov A et al. (1995) 5S rRNA gene hybridizes to human chromosome 1 at two sites (1q42.11-q42.13 and 1q43). Cytogenet Cell Genet 68: 82-84.Google Scholar
  39. Lazar E, Haendler B, Jacob M (1983) Two 5S genes are expressed in chicken somatic cells. Nucleic Acids Res 11: 7735-7741.Google Scholar
  40. Little RD, Braaten DC (1989) Genomic organization of human 5S rDNA and sequence of one tandem repeat. Genomics 4: 376-383.Google Scholar
  41. Lomholt B, Frederiksen S, Nielsen J, Hallenberg C (1995) Additional assignment of the human 5S rRNA genes to chromosome region 1q31. Cytogenet Cell Genet 70: 76-79.Google Scholar
  42. Lomholt B, Christensen K, Frederiksen S (2001) Syrian hamster 5S rRNA genes are assigned to 6q2 with PNA-FISH by an R-banded karyotype. Cytogenet Cell Genet 94: 169-172.Google Scholar
  43. Martins C, Galetti PM Jr (2001) Organization of 5S rDNA in species of the fish Leporinus: two different genomic locations are characterized by distinct nontranscribed spacers. Genome 44: 903-910.Google Scholar
  44. Mashkova T, Oparina N, Alexandrov I et al. (1998) Unequal cross-over is involved in human alpha satellite DNA rearrangements on a border of the satellite domain. FEBS Lett 441: 451-457.Google Scholar
  45. Matsuda Y, Moriwaki K, Chapman V et al. (1994) Chromosomal mapping of mouse 5S rRNA genes by direct R-banding fluorescence in situ hybridization. Cytogenet Cell Genet 66: 246-249.Google Scholar
  46. McMahon ME, Stamenkovich D, Petes TD (1984) Tandemly arranged variant 5S ribosomal RNA genes in the yeast Saccharomyces cerevisiae. Nucleic Acids Res 12: 8001-8016.Google Scholar
  47. Miller JR, Cartwright EM, Brownlee GG, Fedoroff NV, Brown DD (1978) The nucleotide sequence of oocyte 5S DNA in Xenopus laevis. II. The GC-rich region. Cell 13: 717-725.Google Scholar
  48. Miller M, Goto R, Taylor R et al. (1996) Assignment of Rfp-Y to the chicken B microchromosome and evidence for high frequency of recombination associated with the nucleolus organizer region. PNAS 93: 3958-3962.Google Scholar
  49. Nielsen J, Hallenberg C, Frederiksen S, SGrensen P, Lomholt B (1993) Transcription of human 5S rRNA genes is influenced by an upstream DNA sequence. Nucleic Acids Res 21: 3631-3636.Google Scholar
  50. Pardue M, Brown D, Birnstiel M (1973) Location of the genes for 5S ribosomal RNA in Xenopus laevis. Chromosoma 42: 191-203.Google Scholar
  51. Phillips R, Reed K (2000) Localization of repetitive DNAs to zebrafish( Danio rerio) chromosomes by fluorescence in situ hybridization (FISH). Chromosome Res 8: 27-35.Google Scholar
  52. Pisenti JM, Delany ME, Taylor RL Jr et al. (2001) Avian genetic resources at risk: An assessment and proposal for conservation of genetic stocks in the USA and Canada. Avian Poult Biol Rev 12: 100-102.Google Scholar
  53. Procunier JD, Dunn RJ (1978) Genetic and molecular organization of the 5S locus and mutants in D. melanogaster. Cell 3: 1087-1093.Google Scholar
  54. Sajdak S, Reed K, Phillips R (1998) Interindividual and interspecies variation in the 5S rDNA of coregonid fish. J Mol Evol 46: 680-688.Google Scholar
  55. Sambrook J, Fritsch E, Maniatis T (1989) Analysis and cloning of eukaryotic genomic DNA. In: Ford N, Nolan C, Ferguson M, eds. Molecular Cloning; A Laboratory Manual. Cold Spring Harbour: Cold Spring Harbor Laboratory Press, pp 9.1-9.59.Google Scholar
  56. Schmid M, Nanda I, Guttenbach M et al. (2000) First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90: 169-218.Google Scholar
  57. Sørensen P, Lomholt B, Frederiksen S, Tommerup N (1991) Fine mapping of human 5S rRNA genes to chromosome 1q42.11 to q42.13. Cytogenet Cell Genet 57: 26-29.Google Scholar
  58. Steffensen D, Duffey P (1974) Localisation of 5S ribosomal RNA genes on human chromosome 1. Nature 252: 741-743.Google Scholar
  59. Suzuki H, Moriwaki K, Sakurai S (1994) Sequences and evolutionary analysis of mouse 5S rDNAs. Mol Biol Evol 11: 704-710.Google Scholar
  60. Suzuki H, Sakurai S, Matsuda Y (1996) Rat 5S rDNA spacer sequences and chromosomal assignment of the genes to the extreme terminal region of chromosome 19. Cytogenet Cell Genet 72: 1-4.Google Scholar
  61. Wimber D, Steffensen D (1970) Localization of 5S RNA genes on Drosophila chromosomes by RNA-DNA hybridization. Science 170: 639-641.Google Scholar
  62. Wimber D, Wimber D (1977) Sites of the 5S ribosomal genes in Drosophila. I. The multiple clusters in the virilis group. Genetics 86: 133-148.Google Scholar
  63. Wingender E, Chen X, Hehl R et al. (2000) TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res 28: 316-319.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Department of Animal ScienceUniversity of CaliforniaDavisUSA

Personalised recommendations