Phylogenetic analysis of mitochondrial substitution rate variation in the angiosperm tribe Sileneae

Abstract

Background: Recent phylogenetic studies have revealed that the mitochondrial genome of the angiosperm Silene noctiflora (Caryophyllaceae) has experienced a massive mutation-driven acceleration in substitution rate, placing it among the fastest evolving eukaryotic genomes ever identified. To date, it appears that other species within Silene have maintained more typical substitution rates, suggesting that the acceleration in S. noctiflora is a recent and isolated evolutionary event. This assessment, however, is based on a very limited sampling of taxa within this diverse genus.

Results: We analyzed the substitution rates in 4 mitochondrial genes (atp1, atp9, cox3 and nad9) across a broad sample of 74 species within Silene and related genera in the tribe Sileneae. We found that S. noctiflora shares its history of elevated mitochondrial substitution rate with the closely related species S. turkestanica. Another section of the genus (Conoimorpha) has experienced an acceleration of comparable magnitude. The phylogenetic data remain ambiguous as to whether the accelerations in these two clades represent independent evolutionary events or a single ancestral change. Rate variation among genes was equally dramatic. Most of the genus exhibited elevated rates for atp9 such that the average tree-wide substitution rate for this gene approached the values for the fastest evolving branches in the other three genes. In addition, some species exhibited major accelerations in atp1 and/or cox3 with no correlated change in other genes. Rates of non-synonymous substitution did not increase proportionally with synonymous rates but instead remained low and relatively invariant.

Conclusion: The patterns of phylogenetic divergence within Sileneae suggest enormous variability in plant mitochondrial mutation rates and reveal a complex interaction of gene and species effects. The variation in rates across genomic and phylogenetic scales raises questions about the mechanisms responsible for the evolution of mutation rates in plant mitochondrial genomes.

Figure 1

Diversity in substitution rates. Synonymous substitution rates per site per billion years (SSB) for different organisms and genomes plotted on a log scale. Black bars represent seed plant mitochondrial genomes. Average rates for animal taxa from Lynch et al. [20]; angiosperm chloroplast and nuclear estimates from Wolfe et al. [74]; mitochondrial rates for individual plant species taken from Cho et al. [5] and Mower et al. [4].

Figure 2

Chronogram showing divergence times estimated in BEAST based on full-length matK coding sequence. Time scale is in millions of years. Error bars at each node show 95% HPD for node age. Values to the right of each node show Bayesian posterior probability and parsimony bootstrap support (in that order) for the corresponding clade. Tree topology was constrained based on 70% parsimony bootstrap consensus.

Figure 3

d_N and d_S trees for mitochondrial genes. Branch lengths are in terms of non-synonymous (d_N) or synonymous (d_S) substitutions per site as estimated by PAML under a constrained topology. The scale is the same for all trees.

Figure 4

Phylogenetic variation in R_S. Branches labelled with absolute synonymous substitution rates and approximate standard errors based on concatenation of nad9, cox3 and atp1. Branch colors indicate fast (red) and slow (blue) rates.