Abstract
Recombination processes acting on tandem arrays are suggested here to have probable intrinsic biases, producing an expected net decrease in array size following each event, in contrast to previous models which assume no net change in array size. We examine the implications of this by modeling copy number dynamics in a tandem array under the joint interactions of sister-strand unequal crossing over (rate γ per generation per copy) and intrastrand recombination resulting in deletion (rate ε per generation per copy). Assuming no gene amplification or selection, the expected mean persistence time of an array starting with z excess copies (i.e., array size z + 1) is z(1 + γ/ε) recombinational events. Nontrivial equilibrium distributions of array sizes exist when gene amplification or certain forms of selection are considered. We characterize the equilibrium distribution for both a simple model of gene amplification and under the assumption that selection imposes a minimal array size, n. For the latter case, n + 1/α is an upper bound for mean array size under fairly general conditions, where α(=2ε/γ) is the scaled deletion rate. Further, the distribution of excess copies over n is bounded above by a geometric distribution with parameter α/(1 + α). Tandem arrays are unlikely to be greatly expanded by unequal crossing over unless α << 1, implying that other mechanisms, such as gene amplification, are likely important in the evolution of large arrays. Thus unequal crossing over, by itself, is likely insufficient to account for satellite DNA.
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- Arnheim N., Krystal M., Schmickel R., Wilson G., Ryder O., Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323–7327. doi: 10.1073/pnas.77.12.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell G. I., Selby M. J., Rutter W. J. The highly polymorphic region near the human insulin gene is composed of simple tandemly repeating sequences. Nature. 1982 Jan 7;295(5844):31–35. doi: 10.1038/295031a0. [DOI] [PubMed] [Google Scholar]
- Brutlag D. L. Molecular arrangement and evolution of heterochromatic DNA. Annu Rev Genet. 1980;14:121–144. doi: 10.1146/annurev.ge.14.120180.001005. [DOI] [PubMed] [Google Scholar]
- Brutlag D., Fry K., Nelson T., Hung P. Synthesis of hybrid bacterial plasmids containing highly repeated satellite DNA. Cell. 1977 Mar;10(3):509–519. doi: 10.1016/0092-8674(77)90038-1. [DOI] [PubMed] [Google Scholar]
- Busby S. J., Reeder R. H. Spacer sequences regulate transcription of ribosomal gene plasmids injected into Xenopus embryos. Cell. 1983 Oct;34(3):989–996. doi: 10.1016/0092-8674(83)90556-1. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Langley C. H., Stephan W. The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics. 1986 Apr;112(4):947–962. doi: 10.1093/genetics/112.4.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devilee P., Slagboom P., Cornelisse C. J., Pearson P. L. Sequence heterogeneity within the human alphoid repetitive DNA family. Nucleic Acids Res. 1986 Mar 11;14(5):2059–2073. doi: 10.1093/nar/14.5.2059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldstein I., Renais J., Scebat L. Experimental nephropathy induced in rabbits by immunization with Escherichia coli 055 lipopolysaccharide. 2. Immunologic findings. Isr J Med Sci. 1980 Aug;16(8):566–571. [PubMed] [Google Scholar]
- Hauswirth W. W., Van de Walle M. J., Laipis P. J., Olivo P. D. Heterogeneous mitochondrial DNA D-loop sequences in bovine tissue. Cell. 1984 Jul;37(3):1001–1007. doi: 10.1016/0092-8674(84)90434-3. [DOI] [PubMed] [Google Scholar]
- Jones R. S., Potter S. S. Characterization of cloned human alphoid satellite with an unusual monomeric construction: evidence for enrichment in HeLa small polydisperse circular DNA. Nucleic Acids Res. 1985 Feb 11;13(3):1027–1042. doi: 10.1093/nar/13.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kato S., Anderson R. A., Camerini-Otero R. D. Foreign DNA introduced by calcium phosphate is integrated into repetitive DNA elements of the mouse L cell genome. Mol Cell Biol. 1986 May;6(5):1787–1795. doi: 10.1128/mcb.6.5.1787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koch A. L. Selection and recombination in populations containing tandem multiplet genes. J Mol Evol. 1979 Dec;14(4):273–285. doi: 10.1007/BF01732495. [DOI] [PubMed] [Google Scholar]
- Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
- Krontiris T. G., DiMartino N. A., Colb M., Parkinson D. R. Unique allelic restriction fragments of the human Ha-ras locus in leukocyte and tumour DNAs of cancer patients. 1985 Jan 31-Feb 6Nature. 313(6001):369–374. doi: 10.1038/313369a0. [DOI] [PubMed] [Google Scholar]
- Lania L., Boast S., Fried M. Excision of polyoma virus genomes from chromosomal DNA by homologous recombination. Nature. 1982 Jan 28;295(5847):349–350. doi: 10.1038/295349a0. [DOI] [PubMed] [Google Scholar]
- Lohe A. R., Brutlag D. L. Multiplicity of satellite DNA sequences in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Feb;83(3):696–700. doi: 10.1073/pnas.83.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melton D. W., McEwan C., McKie A. B., Reid A. M. Expression of the mouse HPRT gene: deletional analysis of the promoter region of an X-chromosome linked housekeeping gene. Cell. 1986 Jan 31;44(2):319–328. doi: 10.1016/0092-8674(86)90766-x. [DOI] [PubMed] [Google Scholar]
- Morris J., Kushner S. R., Ivarie R. The simple repeat poly(dT-dG).poly(dC-dA) common to eukaryotes is absent from eubacteria and archaebacteria and rare in protozoans. Mol Biol Evol. 1986 Jul;3(4):343–355. doi: 10.1093/oxfordjournals.molbev.a040399. [DOI] [PubMed] [Google Scholar]
- Nagylaki T., Petes T. D. Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics. 1982 Feb;100(2):315–337. doi: 10.1093/genetics/100.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nussinov R. Strong adenine clustering in nucleotide sequences. J Theor Biol. 1980 Jul 21;85(2):285–291. doi: 10.1016/0022-5193(80)90021-1. [DOI] [PubMed] [Google Scholar]
- Ohta T. Genetic variation in small multigene families. Genet Res. 1981 Apr;37(2):133–149. doi: 10.1017/s0016672300020115. [DOI] [PubMed] [Google Scholar]
- Perelson A. S., Bell G. I. Mathematical models for the evolution of multigene families by unequal crossing over. Nature. 1977 Jan 27;265(5592):304–310. doi: 10.1038/265304a0. [DOI] [PubMed] [Google Scholar]
- Roth G. E., Moritz K. B. Restriction enzyme analysis of the germ line limited DNA of Ascaris suum. Chromosoma. 1981;83(2):169–190. doi: 10.1007/BF00286787. [DOI] [PubMed] [Google Scholar]
- Saedler H., Nevers P. Transposition in plants: a molecular model. EMBO J. 1985 Mar;4(3):585–590. doi: 10.1002/j.1460-2075.1985.tb03670.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schimke R. T. Gene amplification in cultured animal cells. Cell. 1984 Jul;37(3):705–713. doi: 10.1016/0092-8674(84)90406-9. [DOI] [PubMed] [Google Scholar]
- Schimke R. T., Sherwood S. W., Hill A. B., Johnston R. N. Overreplication and recombination of DNA in higher eukaryotes: potential consequences and biological implications. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2157–2161. doi: 10.1073/pnas.83.7.2157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwarz-Sommer Z., Gierl A., Cuypers H., Peterson P. A., Saedler H. Plant transposable elements generate the DNA sequence diversity needed in evolution. EMBO J. 1985 Mar;4(3):591–597. doi: 10.1002/j.1460-2075.1985.tb03671.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slightom J. L., Chang L. Y., Koop B. F., Goodman M. Chimpanzee fetal G gamma and A gamma globin gene nucleotide sequences provide further evidence of gene conversions in hominine evolution. Mol Biol Evol. 1985 Sep;2(5):370–389. doi: 10.1093/oxfordjournals.molbev.a040357. [DOI] [PubMed] [Google Scholar]
- Solomon M. J., Strauss F., Varshavsky A. A mammalian high mobility group protein recognizes any stretch of six A.T base pairs in duplex DNA. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1276–1280. doi: 10.1073/pnas.83.5.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Southern E. M. Long range periodicities in mouse satellite DNA. J Mol Biol. 1975 May 5;94(1):51–69. doi: 10.1016/0022-2836(75)90404-0. [DOI] [PubMed] [Google Scholar]
- Stephan W. Recombination and the evolution of satellite DNA. Genet Res. 1986 Jun;47(3):167–174. doi: 10.1017/s0016672300023089. [DOI] [PubMed] [Google Scholar]
- Strauss F., Varshavsky A. A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell. 1984 Jul;37(3):889–901. doi: 10.1016/0092-8674(84)90424-0. [DOI] [PubMed] [Google Scholar]
- Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb Symp Quant Biol. 1966;31:77–84. doi: 10.1101/sqb.1966.031.01.014. [DOI] [PubMed] [Google Scholar]
- Tautz D., Trick M., Dover G. A. Cryptic simplicity in DNA is a major source of genetic variation. Nature. 1986 Aug 14;322(6080):652–656. doi: 10.1038/322652a0. [DOI] [PubMed] [Google Scholar]
- Wilkins A. S. Eukaryotic chromosome replication and the radial loop model. J Theor Biol. 1981 Apr 21;89(4):715–717. doi: 10.1016/0022-5193(81)90038-2. [DOI] [PubMed] [Google Scholar]
- Willard C., Wong E., Hess J. F., Shen C. K., Chapman B., Wilson A. C., Schmid C. W. Comparison of human and chimpanzee zeta 1 globin genes. J Mol Evol. 1985;22(4):309–315. doi: 10.1007/BF02115686. [DOI] [PubMed] [Google Scholar]
- Yavachev L. P., Georgiev O. I., Braga E. A., Avdonina T. A., Bogomolova A. E., Zhurkin V. B., Nosikov V. V., Hadjiolov A. A. Nucleotide sequence analysis of the spacer regions flanking the rat rRNA transcription unit and identification of repetitive elements. Nucleic Acids Res. 1986 Mar 25;14(6):2799–2810. doi: 10.1093/nar/14.6.2799. [DOI] [PMC free article] [PubMed] [Google Scholar]