Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants

Abstract

Plant mitochondrial (mt) genomes have long been known to evolve slowly in sequence. Here we show remarkable departure from this pattern of conservative evolution in a genus of flowering plants. Substitution rates at synonymous sites vary substantially among lineages within Plantago. At the extreme, rates in Plantago exceed those in exceptionally slow plant lineages by approximately 4,000-fold. The fastest Plantago lineages set a new benchmark for rapid evolution in a DNA genome, exceeding even the fastest animal mt genome by an order of magnitude. All six mt genes examined show similarly elevated divergence in Plantago, implying that substitution rates are highly accelerated throughout the genome. In contrast, substitution rates show little or no elevation in Plantago for each of four chloroplast and three nuclear genes examined. These results, combined with relatively modest elevations in rates of nonsynonymous substitutions in Plantago mt genes, indicate that major, reversible changes in the mt mutation rate probably underlie the extensive variation in synonymous substitution rates. These rate changes could be caused by major changes in any number of factors that control the mt mutation rate, from the production and detoxification of oxygen free radicals in the mitochondrion to the efficacy of mt DNA replication and/or repair.

Fig. 2.

Estimates of phylogeny, divergence times, and R_S values in the Plantaginaceae. (A and B) ML trees of Plantaginaceae (A) and subgenus Plantago (B) were based on four and six chloroplast regions, respectively. Numbers indicate bootstrap support from 1,000 ML replicates. Seven outgroup species were included in the analysis in A but are not shown. (C and D) Chronograms of Plantaginaceae based on the topology found in A (C), and the topology found in B (D) (see Materials and Methods). Internal nodes are labeled A–J. Values above each branch indicate mean R_S in SSB from Table 1 for that branch.

Fig. 1.

Substitution rates in Plantago are highly elevated and variable in mt genes compared with chloroplast (cp) and nuclear (nc) genes. Shown are topologically constrained ML trees based on synonymous (d_S) or nonsynonymous (d_N) sites for protein genes (all drawn to the same scale) or all sites for SSU rDNA. The three mt trees at left differ from the three boxed (Top Inset, Middle Inset, and Bottom Inset) trees only according to the constraints placed on subgenus Plantago (constrained as shown in Fig. 2 B and A, respectively). Note that the picture of highly elevated and variable R_S in Plantago evident in these trees was observed for both unconstrained and constrained trees (Fig. 6) indicating that our findings are not an artifact of topological constraints. Taxa within Plantago are color-coded by subgenus. Pl, subgenus Plantago; Co, Coronopus; Ps, Psyllium. Mt gene trees were based on 1,341 (cox1), 1,272 (atp1), and 1,401 (SSU rDNA) nt; chloroplast gene trees were based on 1,317 (rbcL) and 1,674 (ndhF) nt; and the nuclear sut1 tree was based on 1,293 nt.