Unprecedented Heterogeneity in the Synonymous Substitution Rate within a Plant Genome

The synonymous substitution rate varies widely among species, but it is generally quite stable within a genome due to the absence of strong selective pressures. In plants, plastid genes tend to evolve faster than mitochondrial genes, rate variation among species generally correlates between the mitochondrial and plastid genomes, and few examples of intragenomic rate heterogeneity exist. To study the extent of substitution rate variation between and within plant organellar genomes, we sequenced the complete mitochondrial and plastid genomes from the bugleweed, Ajuga reptans, which was previously shown to exhibit rate heterogeneity for several mitochondrial genes. Substitution rates were accelerated specifically in the mitochondrial genome, which contrasts with correlated plastid and mitochondrial rate changes in most other angiosperms. Strikingly, we uncovered a 340-fold range of synonymous substitution rate variation among Ajuga mitochondrial genes. This is by far the largest amount of synonymous rate heterogeneity ever reported for a genome, but the evolutionary forces driving this phenomenon are unclear. Selective effects on synonymous sites in plant mitochondria are generally weak and thus unlikely to generate such unprecedented intragenomic rate heterogeneity. Quickly evolving genes are not clustered in the genome, arguing against localized hypermutation, although it is possible that they were clustered ancestrally given the high rate of genomic rearrangement in plant mitochondria. Mutagenic retroprocessing, involving error-prone reverse transcription and genomic integration of mature transcripts, is hypothesized as another potential explanation.