High apparent rate of simultaneous compensatory base-pair substitutions in ribosomal RNA.

We present a model for the evolution of paired bases in RNA sequences. The new model allows for the instantaneous rate of substitution of both members of a base pair in a compensatory substitution (e.g., A-U-->G-C) and expands our previous work by allowing for unpaired bases or noncanonical pairs. We implemented the model with distance and maximum likelihood methods to estimate the rates of simultaneous substitution of both bases, alphad, vs. rates of substitution of individual bases, alphas in rRNA. In the rapidly evolving D2 expansion segments of Drosophila large subunit rRNA, we estimate a low ratio of alphad/alphas, indicating that most compensatory substitutions involve a G-U intermediate. In contrast, we find a surprisingly high ratio of alphad/alphas in the core small subunit rRNA, indicating that the evolution of the slowly evolving rRNA sequences is modeled much more accurately if simultaneous substitution of both members of a base pair is allowed to occur approximately as often as substitution of individual bases. Using simulations, we have ruled out several potential sources of error in the estimation of alphad/alphas. We conclude that in the core rRNA sequences compensatory substitutions can be fixed so rapidly as to appear to be instantaneous.

[1]  W. Brown,et al.  Rates and patterns of base change in the small subunit ribosomal RNA gene. , 1993, Genetics.

[2]  Ross A. Overbeek,et al.  The Ribosomal Database Project (RDP) , 1996, Nucleic Acids Res..

[3]  A. Rzhetsky.  Estimating substitution rates in ribosomal RNA genes. , 1995, Genetics.

[4]  W. Stephan.  The rate of compensatory evolution. , 1996, Genetics.

[5]  S. Muse.  Evolutionary analyses of DNA sequences subject to constraints of secondary structure. , 1995, Genetics.

[6]  A. von Haeseler,et al.  A stochastic model for the evolution of autocorrelated DNA sequences. , 1994, Molecular phylogenetics and evolution.

[7]  F Rousset,et al.  Evolution of compensatory substitutions through G.U intermediate state in Drosophila rRNA. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Hillis,et al.  Ribosomal DNA: Molecular Evolution and Phylogenetic Inference , 1991, The Quarterly Review of Biology.

[9]  W. Wheeler,et al.  Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. , 1988, Molecular biology and evolution.

[10]  D. Hillis,et al.  Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. , 1993, Molecular biology and evolution.

[11]  Ross A. Overbeek,et al.  The ribosomal database project , 1992, Nucleic Acids Res..

[12]  E. Tillier,et al.  Neighbor Joining and Maximum Likelihood with RNA Sequences: Addressing the Interdependence of Sites , 1995 .

[13]  H. Noller.  Structure of ribosomal RNA. , 1984, Annual review of biochemistry.

[14]  G. Olsen,et al.  Ribosomal RNA: a key to phylogeny , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  R. Gutell,et al.  Collection of small subunit (16S- and 16S-like) ribosomal RNA structures: 1994. , 1993, Nucleic acids research.