Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes

Abstract

A comparative analysis of the transfer RNA genes in the genomes of the major kingdoms of eukaryotes and prokaryotes leads to the general conclusion that the rate of evolution of organelle tRNA genes is typically equal to or greater than that of their nuclear counterparts. Situations where this is not the case, most notably in vascular plants, are attributable to an elevated mutation rate in the nuclear genome. Through a comparison of rates of mutation with rates of nucleotide substitution, it is shown that there is a reduction in the efficiency of selection on new mutations in organelle genes. Numerous lines of evidence, including observed reductions in stem duplex stability and changes in loop sizes, suggest that the excess changes observed in the organelle genes are mildly deleterious. Uniparental inheritance of organelles causes a reduction in the efficiency of selection through the joint effects of an increase in linkage disequilibrium and a decrease in effective population size. These results provide molecular support for the idea that asexually propagating genomes are subject to long-term, gradual fitness loss and raise questions about the role of organelle mutations in the long-term survival of major phylogenetic lineages.