Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs.

Abstract

Comparison of plant mitochondrial (mt), chloroplast (cp) and nuclear (n) DNA sequences shows that the silent substitution rate in mtDNA is less than one-third that in cpDNA, which in turn evolves only half as fast as plant nDNA. The slower rate in mtDNA than in cpDNA is probably due to a lower mutation rate. Silent substitution rates in plant and mammalian mtDNAs differ by one or two orders of magnitude, whereas the rates in nDNAs may be similar. In cpDNA, the rate of substitution both at synonymous sites and in noncoding sequences in the inverted repeat is greatly reduced in comparison to single-copy sequences. The rate of cpDNA evolution appears to have slowed in some dicot lineages following the monocot/dicot split, and the slowdown is more conspicuous at nonsynonymous sites than at synonymous sites.Our current knowledge of the rates and mechanisms of molecular evolution has been derived largely from comparative studies of genes and proteins of animals (1, 2). Only recently has the study of the molecular biology of plants provided sufficient data to allow the evolution of plant genes to be investigated. Since the plant and animal kingdoms diverged about 1000 million years (Myr) ago, their patterns of evolution might have become very different. In fact, plants differ from animals in the organization oftheir organelle DNA by having a much larger and structurally more variable mitochondrial genome and by having a third (chloroplast) genome (3). So, do the rates of nucleotide substitution differ between animal and plant DNAs? Also, since in mammals mitochondrial DNA (mtDNA) evolves much faster than nuclear DNA (nDNA) (4), do the substitution rates vary greatly among the three plant genomes?Previous studies based on a few gene sequences or on restriction enzyme mapping have suggested that chloroplast genes have lower rates of nucleotide substitution than mammalian nuclear genes (3, 5) and that plant mtDNA evolves slowly in nucleotide sequence, though it undergoes frequent rearrangement (6). Restriction analysis (3, 7) has also suggested that the large inverted repeat (IR) sequences in chloroplast DNA (cpDNA) have lower rates of nucleotide substitution than the rest of the chloroplast genome. Available DNA sequence data from plants now allow a detailed investigation of the rates of nucleotide substitution in the three plant genomes, reconstruction of the phylogenetic relationships among some higher plants, and comparison of evolutionary rates among lineages.MATERIALS AND METHODS DNA sequences were taken from GenBank § and the literature; the sequences of liverwort and tobacco chloroplast genomes (8, 9) were kindly provided on disk by K. Ohyama and M. Sugiura.Numbers of nucleotide substitutions in noncoding sequences were calculated by the two-parameter method of Kimura (1); regions in which the correct alignment was not apparent were excluded from the analysis. Protein-coding genes were analyzed by the method of Li et al. (10) RESULTSRates of Evolution of the Three Plant Genomes. In Table 1 we compare the ...

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