Molecular Biology and Evolution, Vol 5, 393-414, Copyright © 1988 by Society for Molecular Biology and Evolution
JM Hancock, D Tautz and GA Dover
This paper examines the effects of DNA sequence evolution on RNA secondary
structures and compensatory mutations. Models of the secondary structures
of Drosophila melanogaster 18S ribosomal RNA (rRNA) and of the complex
between 2S, 5.8S, and 28S rRNAs have been drawn on the basis of comparative
and energetic criteria. The overall AU richness of the D. melanogaster
rRNAs allows the resolution of some ambiguities in the structures of both
large rRNAs. Comparison of the sequence of expansion segment V2 in D.
melanogaster 18S rRNA with the same region in three other Drosophila
species and the tsetse fly (Glossina morsitans morsitans) allows us to
distinguish between two models for the secondary structure of this region.
The secondary structures of the expansion segments of D. melanogaster 28S
rRNA conform to a general pattern for all eukaryotes, despite having highly
divergent sequences between D. melanogaster and vertebrates. The 70 novel
compensatory mutations identified in the 28S rRNA show a strong (70%) bias
toward A-U base pairs, suggesting that a process of biased mutation and/or
biased fixation of A and T point mutations or AT-rich slippage-generated
motifs has occurred during the evolution of D. melanogaster rDNA. This
process has not occurred throughout the D. melanogaster genome. The
processes by which compensatory pairs of mutations are generated and spread
are discussed, and a model is suggested by which a second mutation is more
likely to occur in a unit with a first mutation as such a unit begins to
spread through the family and concomitantly through the population.
Alternatively, mechanisms of proofreading in stem-loop structures at the
DNA level, or between RNA and DNA, might be involved. The apparent
tolerance of noncompensatory mutations in some stems which are otherwise
strongly supported by comparative criteria within D. melanogaster 28S rRNA
must be borne in mind when compensatory mutations are used as a criterion
in secondary-structure modeling. Noncompensatory mutation may extend to the
production of unstable structures where a stem is stabilized by RNA-
protein or additional RNA-RNA interactions in the mature ribosome. Of
motifs suggested to be involved in rRNA processing, one (CGAAAG) is
strongly overrepresented in the 28S rRNA sequence. The data are discussed
both in the context of the forces involved with the evolution of multigene
families and in the context of molecular coevolution in the rDNA family in
particular.
ORIGINAL ARTICLE
Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster
Genetics Department, University of Cambridge, United Kingdom.
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