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PMID: 6261251 Published · ppublish English Comparative Study Journal Article

Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes.

Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E

Abstract

We have found that human and ape ribosomal genes undergo concerted evolution involving genetic exchanges among nucleolus organizers on nonhomologous chromosomes. This conclusion is based upon restriction enzyme analysis of the ribosomal gene families in man and five ape species. Certain structural features were found to differ among (but not within) species even though the ribosomal genes have a multichromosomal distribution. Genetic exchanges among nucleolus organizer regions may be related to the well-known phenomenon of acrocentric chromosome associations observed in man and apes. Length variation in a region of the nontranscribed spacer was found in both chimpanzee species we examined. The nature of this length variation was found to be identical to that previously described in man. The origin of the length variation and its polymorphism within these three species might be explained by unequal alignment and unequal cross-over among the ribosomal genes. An especially surprising finding was a nucleotide sequence polymorphism present in each individual human and ape we examined. Some ribosomal genes of each individual have a HindII site in the 28S gene about 800 base pairs from the EcoRI site in this gene. The remaining 28S genes lack this HindII site. The presence of this polymorphism within individuals of every species we examined suggests that it has been maintained by natural selection.

MeSH Terms
Animals Biological Evolution Crossing Over, Genetic DNA Restriction Enzymes/metabolism Hominidae/genetics Humans Molecular Weight Nucleolus Organizer Region/ultrastructure Polymorphism, Genetic RNA, Ribosomal/genetics Transcription, Genetic
Chemicals
RNA, Ribosomal DNA Restriction Enzymes
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Arnheim N
Krystal M
Schmickel R
Wilson G
Ryder O
Zimmer E
References (50)
50 references, click to expand
  1. A restriction enzyme from Hemophilus influenzae. II.
    J Mol Biol. 1970 Jul 28;51(2):393-409 PMID: 5312501
  2. Retention of common nucleotide sequences in the ribosomal deoxyribonucleic acid of eukaryotes and some of their physical characteristics.
    Biochemistry. 1971 Jul 6;10(14):2761-9 PMID: 5105183
  3. Iodination of nucleic acids in vitro.
    Biochemistry. 1971 May 25;10(11):1993-2000 PMID: 4935105
  4. A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes.
    J Mol Biol. 1972 Jan 14;63(1):57-73 PMID: 5016971
  5. The ribosomal RNA cistrons.
    Prog Nucleic Acid Res Mol Biol. 1971;11:351-89 PMID: 5004308
  6. Location of ribosomal DNA in the human chromosome complement.
    Proc Natl Acad Sci U S A. 1972 Nov;69(11):3394-8 PMID: 4508329
  7. Quantitation of human ribosomal DNA: hybridization of human DNA with ribosomal RNA for quantitation and fractionation.
    Pediatr Res. 1973 Jan;7(1):5-12 PMID: 4687000
  8. Localization of rDNA in the chimpanzee (Pan troglodytes) chromosome complement.
    Chromosoma. 1974;46(4):435-41 PMID: 4859400
  9. Neutral evolution and immunoglobulin diversity.
    Nature. 1974 Jul 26;250(464):327-8 PMID: 4853332
  10. Localization of rDNA and Giemsa-banded chromosome complement of white-handed gibbon, Hylobates lar.
    Chromosoma. 1975;51(1):35-40 PMID: 49260
  11. Changes in size and secondary structure of the ribosomal transcription unit during vertebrate evolution.
    J Mol Biol. 1975 May 25;94(3):503-17 PMID: 809590
  12. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  13. The organization, expression, and evolution of antibody genes and other multigene families.
    Annu Rev Genet. 1975;9:305-53 PMID: 813561
  14. Redundant genes.
    Annu Rev Genet. 1975;9:355-85 PMID: 1108767
  15. Evolution of repeated DNA sequences by unequal crossover.
    Science. 1976 Feb 13;191(4227):528-35 PMID: 1251186
  16. Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila.
    Nature. 1976 Sep 2;263(5572):27-30 PMID: 822350
  17. The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis.
    J Mol Biol. 1976 Aug 25;105(4):461-86 PMID: 787539
  18. Detection of nucleolus organizer regions in chromosomes of human, chimpanzee, gorilla, orangutan and gibbon.
    Chromosoma. 1976 Jun 30;56(1):15-27 PMID: 61844
  19. Acrocentric chromosome associations in man.
    Am J Hum Genet. 1976 Nov;28(6):567-76 PMID: 795295
  20. Chromosomal distribution of rDNA in Pan paniscus, Gorilla gorilla beringei, and Symphalangus syndactylus: comparison to related primates.
    Chromosoma. 1976 Dec 16;59(2):147-55 PMID: 1009815
  21. Mathematical models for the evolution of multigene families by unequal crossing over.
    Nature. 1977 Jan 27;265(5592):304-10 PMID: 834278
  22. The structural organization of ribosomal DNA in Drosophila melanogaster.
    Cell. 1977 Feb;10(2):193-212 PMID: 402222
  23. Restriction analysis of the nontranscribed spacers of Xenopus laevis ribosomal DNA.
    Cell. 1977 Jul;11(3):599-607 PMID: 560255
  24. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I.
    J Mol Biol. 1977 Jun 15;113(1):237-51 PMID: 881736
  25. Heterogeneity of the ribosomal genes in mice and men.
    Cell. 1977 Jun;11(2):363-70 PMID: 560912
  26. Frequency of satellite association of human chromosomes is correlated with amount of Ag-staining of the nucleolus organizer region.
    Am J Hum Genet. 1977 Sep;29(5):490-502 PMID: 70995
  27. A physical map of the DNA regions flanking the rabbit beta-globin gene.
    Cell. 1977 Oct;12(2):429-39 PMID: 912752
  28. Enhanced autoradiographic detection of 32P and 125I using intensifying screens and hypersensitized film.
    FEBS Lett. 1977 Oct 15;82(2):314-6 PMID: 913604
  29. A new restriction endonuclease from Streptomyces albus G.
    J Mol Biol. 1978 Jan 5;118(1):127-35 PMID: 415144
  30. X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions.
    Cell. 1978 Jun;14(2):269-78 PMID: 96940
  31. Molecular analysis of cloned human 18S ribosomal DNA segments.
    Proc Natl Acad Sci U S A. 1978 Nov;75(11):5367-71 PMID: 364477
  32. Polymorphism of DNA sequence adjacent to human beta-globin structural gene: relationship to sickle mutation.
    Proc Natl Acad Sci U S A. 1978 Nov;75(11):5631-5 PMID: 281713
  33. Length heterogeneity in a region of the human ribosomal gene spacer is not accompanied by extensive population polymorphism.
    J Mol Biol. 1978 Nov 25;126(1):91-104 PMID: 739545
  34. Ribosomal DNA in Drosophila melanogaster. II. Heteroduplex mapping of cloned and uncloned rDNA.
    J Mol Biol. 1978 Dec 25;126(4):769-82 PMID: 106129
  35. Rare bases in animal DNA.
    Nature. 1970 Mar 7;225(5236):948-9 PMID: 4391887
  36. Construction and characterization of the hybrid bacteriophage lambda Charon vectors for DNA cloning.
    J Virol. 1979 Feb;29(2):555-75 PMID: 372561
  37. The chromosomal location of rDNA in the Sumatran orangutan, Pongo pygmaeus albei.
    Cytogenet Cell Genet. 1979;23(3):213-6 PMID: 436453
  38. Satellite DNA and heterochromatin variants: the case for unequal mitotic crossing over.
    Hum Genet. 1979 Mar 12;47(2):169-86 PMID: 374224
  39. Isolation and sequence organization of human ribosomal DNA.
    J Mol Biol. 1979 Mar 5;128(3):289-303 PMID: 439136
  40. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila.
    Cell. 1979 Jul;17(3):597-605 PMID: 113105
  41. Evolution of transcribed and spacer sequences in the ribosomal RNA genes of Drosophila.
    Cell. 1979 Jul;17(3):607-14 PMID: 113106
  42. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683-7 PMID: 291033
  43. Characterization of mouse ribosomal gene fragments purified by molecular cloning.
    Gene. 1979 Oct;7(2):83-96 PMID: 159852
  44. The genetic behaviour of a cloned mouse ribosomal DNA segment mimics mouse ribosomal gene evolution.
    J Mol Biol. 1979 Nov 15;134(4):743-63 PMID: 231673
  45. Rectification of tandemly repetitious DNA. II. Clustering and periodicity.
    J Theor Biol. 1979 Nov 21;81(2):275-88 PMID: 537372
  46. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158-62 PMID: 6929543
  47. Repeated genes in eukaryotes.
    Annu Rev Biochem. 1980;49:727-64 PMID: 6996571
  48. Nucleolus-organisers in the causation of chromosomal anomalies in man.
    Lancet. 1961 Jul 15;2(7194):123-6 PMID: 13730523
  49. Distribution of 5-methylcytosine in pyrimidine sequences of deoxyribonucleic acids.
    Biochim Biophys Acta. 1962 Jun 11;55:953-9 PMID: 13887466
  50. SPECIFIC DUPLEX FORMATION IN VITRO OF MAMMALIAN DNA.
    J Mol Biol. 1965 Jun;12:394-409 PMID: 14337503
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1980-12-00
Pages
7323-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC350495
Subset
IM
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