Abstract
The genomes of Old-World, New-World, and prosimian primates contain members of a large class of highly repetitive DNAs that are related to one another and to component α DNA of the African green monkey by their sequence homologies and restriction site periodicities. The members, of this class of highly repetitive DNAs are termed the alphoid DNAs, after the prototypical member, component α of the African green monkey which was the first such DNA to be identified (Maio, 1971) and sequenced (Rosenberg et al., 1978). The alphoid DNAs appear to be uniquely primate sequences. — From the restriction enzyme cleavage patterns and Southern blot hybridizations under different stringency conditions, the alphoid DNAs comprise multiple sequence families exhibiting varying degrees of homology to component α DNA. They also share common elements in their restriction site periodicities (172 · n base-pairs), in the long-range organization of their repeating units, and in their banding behavior in CsCl and Cs2SO4 buoyant density gradients, in which they band within the bulk DNA as cryptic repetitive components. — In the three species from the Family Cercopithecidae examined, the alphoid DNAs represent the most abundant, tandemly repetitive sequence components, comprising about 24% of the African green monkey genome and 8 to 10% of the Rhesus monkey and baboon genomes. In restriction digests, the bulk of the alphoid DNAs among the Cercopithecidae appeared quantitatively reduced to a simple series of arithmetic segments based on a 172 base-pair (bp) repeat. In contrast with these simple restriction patterns, complex patterns were observed when human alphoid DNAs were cleaved with restriction enzymes. Detailed analysis revealed that the human genome contains multiple alphoid sequence families which differ from one another both in their repeat sequence organization and in their degree of homology to the African green monkey component α DNA. — The finding of alphoid sequences in other Old-World primate families, in a New-World monkey, and in a prosimian primate attests to the antiquity of these sequences in primate evolution and to the sequence conservatism of a large class of mammalian highly repetitive DNA. In addition, the relative conservatism exhibited by these sequences may distinguish the alphoid DNAs from more recently evolved highly repetitive components and satellite DNAs which have a more restricted taxonomical distribution.
Similar content being viewed by others
References
Breathnach, R., Benoist, C., O'Hare, K., Gannon, F., Chambon, P.: Ovalbumin gene: Evidence for a leader sequence in mRNA and DNA sequences at the exon-intron boundaries. Proc. nat. Acad. Sci. (Wash.) 75, 4853–4857 (1978)
Britten, R.J., Davidson, E.H.: Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Quart. Rev. Biol. 46, 111–138 (1971)
Brown, D.D., Sugimoto, K.: The structure and evolution of ribosomal and 5S DNAs of Xenopus laevis and Xenopus mulleri. Cold Spr. Harb. Symp. quant. Biol. 38, 501–505 (1973)
Brown, F.L., Musich, P.R., Maio, J.J.: The repetitive sequence structure of component α DNA and its relationship to the nucleosomes of the African green minkey. J. molec. Biol. 131, 777–799 (1979)
Chiarelli, A.B.: Evolution of the Primates. London-New York: Academic Press 1973
Craig-Holmes, A.P., Shaw, M.W.: Polymorphisms of human constitutive heterochromatin. Science 174, 702–704 (1971)
Denhardt, D.: A membrane-filter technique for the detection of complementary DNA. Biochem. biophys. Res. Commun. 23, 641–646 (1966)
Donehower, L., Furlong, C., Gillespie, D., Kurnit, D.: DNA sequence of baboon highly-repeated DNA: Evidence for evolution by unequal mitotic exchanges. Proc. nat. Acad. Sci. (Wash.) 77, 2129–2133 (1980)
Fittler, R.: Analysis of the α-satellite DNA from African green monkey cells by restriction nucleases. Europ. J. Biochem. 74, 343–352 (1977)
Fry, K., Salser, W.: Nucleotide sequences of HS-α satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12, 1069–1084 (1977)
Gosden, J.R., Mitchell, A.R., Seuanez, H.N., Gosden, C.M.: The distribution of sequences complementary to human satellite DNAs I, II and IV. in the chromosomes of chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla) and orang utan (Pongo pygmaeus). Chromosoma (Berl.) 63, 253–271 (1977a)
Gosden, J.R., Mitchell, A.R., Seuanez, H.N.: Localization of sequences complementary to human satellite DNAs in man and the hominoid apes. In: Human cytogenetics: ICN-UCLA Symposia on molecular and cellular biology, VII, pp. 75–85. New York: Academic Press 1977b
Grouchy de, J., Turleau, C., Finaz, C.: Chromosome phylogeny of the primates. Ann. Rev. Genet. 12, 289–328 (1978)
Hennig, W., Walker, P.M.B.: Variations in the DNA from two rodent families (Cricetidae and Muridae). Nature (Lond.) 225, 915–919 (1970)
Jeffreys, A.J., Flavell, R.A.: A physical map of the DNA regions flanking the rabbit β-globin gene. Cell 8, 429–439 (1977)
Jeppesen, P.G.N., Sanders, L., Slocombe, P.M.: A restriction cleavage map of φX174 DNA by pulse-chase labelling using E. coli DNA polymerase. Nucleic Acids Res. 3, 1323–1339 (1976)
Jones, K.W.: Annotation: Satellite DNA. J. med. Genet. 10, 273–281 (1973)
Jones, K.W., Purdom, I.F.: Evolution of defined classes of human and primate DNA. In: Chromosome variations in human evolution (A.J. Boyce, ed.). p. 39–51. London: Taylor and Francis 1975
King, M.C., Wilson, A.C.: Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975)
Kurnit, D.M.: Satellite DNA and heterochromatin variants: The case for unequal mitotic crossing over. Hum. Genet. 47, 169–186 (1979)
Kurnit, D.M., Maio, J.J.: Subnuclear redistribution of DNA species in confluent and growing mammalian cells. Chromosoma (Berl.) 42, 23–36 (1973)
Kurnit, D.M., Maio, J.J.: Variable satellite DNAs in the African green monkey Cercopithecus aethiops. Chromosoma (Berl.) 45, 387–400 (1974)
Laskey, R.A., Mills, A.D.: Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Europ. J. Biochem. 56, 335–341 (1975)
Maio, J.J.: DNA strand reassociation and polyribonucleotide binding in the African green monkey, Cercopithecus aethiops. J. molec. Biol. 56, 579–595 (1971)
Maio, J.J., Brown, F.L., Musich, P.R.: Subunit structure of chromatin and the organization of eukaryotic highly repetitive DNA: Recurrent periodicities and models for the evolutionary origins of repetitive DNA. J. molec. Biol. 117, 637–655 (1977)
Maniatis, T.A., Jeffrey, A., Klied, D.G.: Nucleotide sequence of the rightward operator of phage λ. Proc. nat. Acad. Sci. (Wash.) 72, 1184–1188 (1975)
Manuelidis, L.: Complex and simple sequences in human repeated DNAs. Chromosoma (Berl.) 66, 1–21 (1978a)
Manuelidis, L.: Chromosomal localization of complex and simple repeated human DNAs. Chromosoma (Berl.) 66, 23–32 (1978b)
Manuelidis, L., Wu, J.C.: Homology between human and simian repeated DNA. Nature (Lond.) 276, 92–94 (1978)
Moar, M.H., Purdon, I.F., Jones, K.W.: Influence of temperature on the detectability and chromosomal distribution of specific DNA sequences by in situ hybridization. Chromosoma (Berl.) 53, 345–359 (1975)
Musich, P.R., Brown, F.L., Maio, J.J.: Subunit structure of chromatin and the organization of eukaryotic highly repetitive DNA: Nucleosomal proteins associated with a highly repetitive mammalian DNA. Proc. nat. Acad. Sci. (Wash.) 74, 3297–3301 (1977a)
Musich, P.R., Maio, J.J., Brown, F.L.: Subunit structure of chromatin and the organization of eukaryotic highly repetitive DNA: Indications of a phase relationship between restriction sites and chromatin subunits in African green monkey and calf nuclei. J. molec. Biol. 177, 657–677 (1977b)
Noll, M.: Differences and similarities in chromatin structure of Neurospora crassa and higher eucaryotes. Cell 8, 349–355 (1976)
Polisky, B., Greene, P., Garfin, D.E., McCarthy, B.J., Goodman, H.M., Boyer, H.W.: Specificity of substrate recognition by the EcoRI restriction endonuclease. Proc. nat. Acad. Sci. (Wash.) 72, 3310–3314 (1975)
Prosser, J., Moar, M., Bobrow, M., Jones, K.W.: Satellite sequences in chimpanzee (Pan troglodytes). Biochim. biophys. Acta (Amst.) 319, 122–134 (1973)
Reddy, V.B., Thimmappaya, B., Dhar, R., Subramanian, K.N., Zain, B.S., Pan, J., Ghosh, P.K., Celma, M.L., Weissmann, S.M.: The genome of simian virus 40. Science 200, 494–502 (1978)
Rigby, P.W.J., Dieckmann, M., Rhodes, C., Berg, P.: Labeling of deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J. molec. Biol. 113, 237–251 (1977)
Rosenberg, H., Singer, M., Rosenberg, M.: Highly reiterated sequences of Simiansimiansimiansimiansimian. Science 200, 394–402 (1978)
Rubin, C.M., Deininger, P.L., Houck, C.M., Schmid, C.W.: A dimer satellite sequence in bonnet monkey DNA consists of distinct monomer subunits. J. molec. Biol. (in press, 1980)
Sakano, H., Huppi, K., Heinrich, G., Tonegawa, S.: Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature (Lond.) 280, 288–294 (1979)
Salser, W.S., Isaacson, J.S.: Mutation rates in globin genes: The genetic load and Haldane's dilemma. Prog. Nucleic Acid. Res. 19, 205–220 (1976)
Sanger, F., Air, G.M., Barrell, B.G., Brown, N.L., Coulson, A.R., Fiddes, J.C., Hutchinson III, C.A., Slocombe, P.M., Smith, M.: Nucleotide sequence of bacteriophage φX174 DNA. Nature (Lond.) 265, 687–695 (1977)
Schildkraut, C.L., Maio, J.J.: Studies on the intranuclear distribution and properties of mouse satellite DNA. Biochim. biophys. Acta (Amst.) 161, 76–93 (1968)
Schildkraut, C.L., Maio, J.J.: Fractions of HeLa DNA differing in their content of guanine + cytosine. J. molec. Biol. 46, 305–315 (1969)
Southern, E.M.: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. molec. Biol. 98, 503–517 (1975)
Tartof, K.D.: Evolution of transcribed and spacer sequences in the ribosomal RNA genes of Drosophila. Cell 17, 607–614 (1979)
van Ooyen, A., van den Berg, J., Mantei, N., Weissmann, C.: Comparison of total sequence of a cloned rabbit β-globin gene and its flanking regions with a homologous mouse sequence. Science 206, 337–344 (1979)
Walker, P.M.B.: “Repetitive” DNA in higher organisms. Prog. Biophys. molec. Biol. 23, 147–190 (1971)
Wuilmart, C., Urbain, J., Givol, D.: On the location of palindromes in immunoglobulin genes. Proc. nat. Acad. Sci. (Wash.) 74, 2526–2530 (1977)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Musich, P.R., Brown, F.L. & Maio, J.J. Highly repetitive component α and related alphoid DNAs in man and monkeys. Chromosoma 80, 331–348 (1980). https://doi.org/10.1007/BF00292688
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00292688