• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Dec 1980; 77(12): 7323–7327.
PMCID: PMC350495

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

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.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Birnstiel ML, Chipchase M, Speirs J. The ribosomal RNA cistrons. Prog Nucleic Acid Res Mol Biol. 1971;11:351–389. [PubMed]
  • Brown DD, Wensink PC, Jordan E. 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. [PubMed]
  • Long EO, Dawid IB. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. [PubMed]
  • Hood L, Campbell JH, Elgin SC. The organization, expression, and evolution of antibody genes and other multigene families. Annu Rev Genet. 1975;9:305–353. [PubMed]
  • Tartof KD. Redundant genes. Annu Rev Genet. 1975;9:355–385. [PubMed]
  • Kurnit DM. Satellite DNA and heterochromatin variants: the case for unequal mitotic crossing over. Hum Genet. 1979 Mar 12;47(2):169–186. [PubMed]
  • Black JA, Gibson D. Neutral evolution and immunoglobulin diversity. Nature. 1974 Jul 26;250(464):327–328. [PubMed]
  • Smith GP. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. [PubMed]
  • Perelson AS, Bell GI. Mathematical models for the evolution of multigene families by unequal crossing over. Nature. 1977 Jan 27;265(5592):304–310. [PubMed]
  • Kirkman HN. Rectification of tandemly repetitious DNA. II. Clustering and periodicity. J Theor Biol. 1979 Nov 21;81(2):275–288. [PubMed]
  • Henderson AS, Warburton D, Atwood KC. Location of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3394–3398. [PMC free article] [PubMed]
  • Henderson A, Warburton D, Atwood KC. Localization of rDNA in the chimpanzee (Pan troglodytes) chromosome complement. Chromosoma. 1974;46(4):435–441. [PubMed]
  • Tantravahi R, Miller DA, Dev VG, Miller OJ. Detection of nucleolus organizer regions in chromosomes of human, chimpanzee, gorilla, orangutan and gibbon. Chromosoma. 1976 Jun 30;56(1):15–27. [PubMed]
  • Henderson AS, Atwood KC, Warburton D. Chromosomal distribution of rDNA in Pan paniscus, Gorilla gorilla beringei, and Symphalangus syndactylus: comparison to related primates. Chromosoma. 1976 Dec 16;59(2):147–155. [PubMed]
  • Schmickel RD. Quantitation of human ribosomal DNA: hybridization of human DNA with ribosomal RNA for quantitation and fractionation. Pediatr Res. 1973 Jan;7(1):5–12. [PubMed]
  • Henderson AS, Warburton D, Megraw-Ripley S, Atwood KC. The chromosomal location of rDNA in the Sumatran orangutan, Pongo pygmaeus albei. Cytogenet Cell Genet. 1979;23(3):213–216. [PubMed]
  • Warburton D, Henderson AS, Atwood KC. Localization of rDNA and Giemsa-banded chromosome complement of white-handed gibbon, Hylobates lar. Chromosoma. 1975;51(1):35–40. [PubMed]
  • OHNO S, TRUJILLO JM, KAPLAN WD, KINOSITA R. Nucleolus-organisers in the causation of chromosomal anomalies in man. Lancet. 1961 Jul 15;2(7194):123–126. [PubMed]
  • Jacobs PA, Mayer M, Morton NE. Acrocentric chromosome associations in man. Am J Hum Genet. 1976 Nov;28(6):567–576. [PMC free article] [PubMed]
  • Miller DA, Tantravahi R, Dev VG, Miller OJ. 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. [PMC free article] [PubMed]
  • Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158–2162. [PMC free article] [PubMed]
  • WALKER PM, MCLAREN A. SPECIFIC DUPLEX FORMATION IN VITRO OF MAMMALIAN DNA. J Mol Biol. 1965 Jun;12:394–409. [PubMed]
  • Kan YW, Dozy AM. 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):5631–5635. [PMC free article] [PubMed]
  • Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed]
  • Commerford SL. Iodination of nucleic acids in vitro. Biochemistry. 1971 May 25;10(11):1993–2000. [PubMed]
  • Rigby PW, Dieckmann M, Rhodes C, Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. [PubMed]
  • Arnheim N. Characterization of mouse ribosomal gene fragments purified by molecular cloning. Gene. 1979 Oct;7(2):83–96. [PubMed]
  • Arnheim N, Kuehn M. The genetic behaviour of a cloned mouse ribosomal DNA segment mimics mouse ribosomal gene evolution. J Mol Biol. 1979 Nov 15;134(4):743–763. [PubMed]
  • Wilson GN, Hollar BA, Waterson JR, Schmickel RD. Molecular analysis of cloned human 18S ribosomal DNA segments. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5367–5371. [PMC free article] [PubMed]
  • Jeffreys AJ, Flavell RA. A physical map of the DNA regions flanking the rabbit beta-globin gene. Cell. 1977 Oct;12(2):429–439. [PubMed]
  • Wahl GM, Stern M, Stark GR. 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):3683–3687. [PMC free article] [PubMed]
  • Laskey RA, Mills AD. Enhanced autoradiographic detection of 32P and 125I using intensifying screens and hypersensitized film. FEBS Lett. 1977 Oct 15;82(2):314–316. [PubMed]
  • Williams BG, Blattner FR. Construction and characterization of the hybrid bacteriophage lambda Charon vectors for DNA cloning. J Virol. 1979 Feb;29(2):555–575. [PMC free article] [PubMed]
  • Schibler U, Wyler T, Hagenbüchle O. Changes in size and secondary structure of the ribosomal transcription unit during vertebrate evolution. J Mol Biol. 1975 May 25;94(3):503–517. [PubMed]
  • Wellauer PK, Dawid IB. Isolation and sequence organization of human ribosomal DNA. J Mol Biol. 1979 Mar 5;128(3):289–303. [PubMed]
  • Krystal M, Arnheim N. 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. [PubMed]
  • Vanyushin BF, Tkacheva SG, Belozersky AN. Rare bases in animal DNA. Nature. 1970 Mar 7;225(5236):948–949. [PubMed]
  • DOSKOCIL J, SORM F. Distribution of 5-methylcytosine in pyrimidine sequences of deoxyribonucleic acids. Biochim Biophys Acta. 1962 Jun 11;55:953–959. [PubMed]
  • Kelly TJ, Jr, Smith HO. A restriction enzyme from Hemophilus influenzae. II. J Mol Biol. 1970 Jul 28;51(2):393–409. [PubMed]
  • Arrand JR, Myers PA, Roberts RJ. A new restriction endonuclease from Streptomyces albus G. J Mol Biol. 1978 Jan 5;118(1):127–135. [PubMed]
  • Arnheim N, Southern EM. Heterogeneity of the ribosomal genes in mice and men. Cell. 1977 Jun;11(2):363–370. [PubMed]
  • Sinclair JH, Brown DD. Retention of common nucleotide sequences in the ribosomal deoxyribonucleic acid of eukaryotes and some of their physical characteristics. Biochemistry. 1971 Jul 6;10(14):2761–2769. [PubMed]
  • Tartof KD, Dawid IG. Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila. Nature. 1976 Sep 2;263(5572):27–30. [PubMed]
  • Endow SA, Glover DM. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell. 1979 Jul;17(3):597–605. [PubMed]
  • Tartof KD. Evolution of transcribed and spacer sequences in the ribosomal RNA genes of Drosophila. Cell. 1979 Jul;17(3):607–614. [PubMed]
  • Wellauer PK, Dawid IB, Tartof KD. X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell. 1978 Jun;14(2):269–278. [PubMed]
  • Wellauer PK, Dawid IB, Brown DD, Reeder RH. The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis. J Mol Biol. 1976 Aug 25;105(4):461–486. [PubMed]
  • Botchan P, Reeder RH, Dawid IB. Restriction analysis of the nontranscribed spacers of Xenopus laevis ribosomal DNA. Cell. 1977 Jul;11(3):599–607. [PubMed]
  • Wellauer PK, Dawid IB. The structural organization of ribosomal DNA in Drosophila melanogaster. Cell. 1977 Feb;10(2):193–212. [PubMed]
  • Wellauer PK, Dawid IB. Ribosomal DNA in Drosophila melanogaster. II. Heteroduplex mapping of cloned and uncloned rDNA. J Mol Biol. 1978 Dec 25;126(4):769–782. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...