Abstract
Six of 204 eukaryotic nuclear small-subunit ribosomal RNA sequences analyzed show a highly significant degree of clustering of short sequence motifs that indicates the fixation of products of replication slippage within them in their recent evolutionary history. A further 72 sequences show weaker indications of sequence repetition. Repetitive sequences in SSU rRNAs are preferentially located in variable regions and in particular in V4 and V7. The conserved region immediately 5′ to V7 (C7) is also consistently repetitive. Whereas variable regions vary in length and appear to have evolved by the fixation of slippage products, C7 shows no indication of length variation. Repetition within C7 is therefore either not a consequence of slippage or reflects very ancient slippage events. The phylogenetic distribution of sequence simplicity in small-subunit rRNAs is patchy, being largely confined to the Mammalia, Apicomplexa, Tetrahymenidae, and Trypanosomatidae. The regions of the molecule associated with sequence simplicity vary with taxonomic grouping as do the sequence motifs undergoing slippage. Comparison of rates of insertion and substitution in a lineage within the genus Plasmodium confirms that both rates are higher in variable regions than in conserved regions. The insertion rate in variable regions is substantially lower than the substitution rate, suggesting that selection acts more strongly on slippage products than on point mutations in these regions. Patterns of coevolution between variable regions may reflect the consequences of selection acting on the incorporation of slippage-derived sequences across the gene.
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Boothroyd JC, Wang A, Campbell DA, Wang CC (1987) An unusually compact ribosomal DNA repeat in the protozoan Giardia lamblia. Nucleic Acids Res 15:4065–4084
Cavalier-Smith T (1985) Introduction: the evolutionary significance of genome size. In: Cavalier-Smith T (ed) The evolution of genome size. John Wiley, New York, pp 1–36
Cavalier-Smith T (1993) Evolution of the eukaryotic genome. In: Broda PMA, Oliver SG, Sims PFG (eds) Society for general microbiology symposium 50: the eukaryotic genome: organization and regulation. Cambridge University Press, Cambridge, pp 333–385
Clark CG, Tague BW, Ware VC, Gerbi SA (1984) Xenopus laevis 28S ribosomal RNA: a secondary structure model and functional implications. Nucleic Acids Res 12:6197–6220
Dallas IF (1992) Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mammal Genome 3:452–456
Dame JB, Sullivan M, McCutchan TF (1984) Two major sequence classes of ribosomal RNA genes in Plasmodium berghei. Nucleic Acids Res 12:5943–5952
Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117
Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Philos Trans R. Soc Lond [Bid] 312:275–289
Engberg J, Nielsen H, Lenaers G, Murayama O, Fujitani H, Higashinakagawa T (1990) Comparison of primary and secondary 26S rRNA structures in two Tetrahymena species: evidence for a strong evolutionary and structural constraint in expansion segments. J Mol Evol 30:514–521
Gonzalez IL, Schmickel RD (1986) The human 18S ribosomal RNA gene: evolution and stability. Am J Hum Genet 38:419–427
Gurell RR (1993) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 21:3051–3054
Hancock JM (1993) Evolution of sequence repetition and gene duplications in the TATA-binding protein TBP (TFIID). Nucleic Acids Res 21:2823–2830
Hancock JM (1994a) Genomic tectonics: slippage-driven tectonic processes in genome evolution. Submitted
Hancock JM (1994b) Consistent patterns of sequence bias in slippage-derived sequences: their origins and consequences for gene and genome evolution. Submitted
Hancock JM, Armstrong JS (1994) SIMPLE34: an improved and enhanced implementation for VAX and Sun computers of the SIMPLE algorithm for analysis of clustered repetitive motifs in nucleotide sequences. Comput Appl Biosci 10:67–70
Hancock JM, Dover GA (1988) Molecular coevolution among crypfically simple expansion segments of eukaryotic 26S/28S rRNAs. Mol Biol Evol 5:377–391
Hancock JM, Dover GA (1990) ‘Compensatory slippage’ in the evolution of ribosomal RNA genes. Nucleic Acids Res 18:5949–5954
Hancock JM, Tautz D, Dover GA (1988) Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. Mol Biol Evol 5:393–414
Kimura M, Obta T (1972) On the stochastic model for estimation of mutational distance between homologous proteins. J Mol Evol 2: 87–90
Kornegay JR, Kocher TD, Williams LA, Wilson AC (1993) Pathways of lysozyme evolution inferred from the sequences of cytochrome b in birds. J Mol Evol 37:367–379
Leipe DD, Gunderson JH, Nerad TA, Sogin ML (1993) Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59:41–48
Larsen N, Olsen GJ, Maidak BL, McCaughey MJ, Overbeek R, Macke TJ, Woese CR (1993) The ribosomal database project. Nucleic Acids Res 21:3021–3023
Musters W, Gonçalves PM, Boon K, Raué HA, van Heerikhuizen H, Planta RJ (1991) The conserved GTPase center and variable region V9 from Saccharomyces cerevisiae 26S rRNA can be replaced by their equivalents from other prokaryotes or eukaryotes without detectable loss of ribosomal function. Proc Natl Acad Sci USA 88: 1469–1473
Neefs J-M, Van de Peer Y, De Rijk P, Chapelle S, De Wachter R (1993) Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res 21:3025–3049
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Rousset F, Pélandakis M, Solignac M (1991) Evolution of compensatory substitutions through G.U intermediate state in Drosophila rRNA. Proc Natl Acad Sci USA 88:10032–10036
Ruiz Linares A, Hancock JM, Dover GA (1991) Secondary structure constraints on the evolution of Drosophila 28S ribosomal RNA expansion segments. J Mol Biol 219:381–390
Sharp PM, Li W-H (1989) On the rate of DNA sequence evolution in Drosophila. J Mol Evol 28:398–402
Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75–77
Staden R (1982) An interactive graphic program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10:2951–2961
Sweeney R, Yao M-C (1989) Identifying functional regions of rRNA by insertion mutagenesis and complete gene replacement in Tetrahymena thermophila. EMBO J 8:933–938
Tautz D, Hancock JM, Webb DA, Tautz C, Dover GA (1988) Complete sequences of the rRNA genes of Drosophila melanogaster. Mol Biol Evol 5:366–376
Tautz D, Trick M, Dover GA (1986) Cryptic simplicity in DNA is a major source of genetic variation. Nature 322:652–656
Unnasch TR, Wirth DF (1983) The avian malaria Plasmodium lophurae has a small number of heterogeneous ribosomal RNA genes. Nucleic Acids Res 11:8443–8459
Van de Peer Y, Neefs J-M, De Rijk P, De Wachter R (1993) Reconstructing evolution from eukaryotic small-ribosomal-subunit RNA sequences: calibration of the molecular clock. J Mol Evol 37:221–232
Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CA (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411–414
Waters AP, Higgins DG, McCutchan TF (1991) Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc Natl Acad Sci USA 88:3140–3144
Waters AP, Higgins DG, McCutchan TF (1993) Evolutionary relatedness of some primate models of Plasmodium. Mol Biol Evol 10: 914–923
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Hancock, J.M. The contribution of DNA slippage to eukaryotic nuclear 18S rRNA evolution. J Mol Evol 40, 629–639 (1995). https://doi.org/10.1007/BF00160511
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DOI: https://doi.org/10.1007/BF00160511