title: Conservative and compensatory evolution in oxidative phosphorylation complexes of angiosperms with highly divergent rates of mitochondrial genome evolution.
abstract: Interactions between nuclear and mitochondrial gene products are critical for eukaryotic cell function. Nuclear genes encoding mitochondrial-targeted proteins (N-mt genes) experience elevated rates of evolution, which has often been interpreted as evidence of nuclear compensation in response to elevated mitochondrial mutation rates. However, N-mt genes may be under relaxed functional constraints, which could also explain observed increases in their evolutionary rate. To disentangle these hypotheses, we examined patterns of sequence and structural evolution in nuclear- and mitochondrial-encoded oxidative phosphorylation proteins from species in the angiosperm genus Silene with vastly different mitochondrial mutation rates. We found correlated increases in N-mt gene evolution in species with fast-evolving mitochondrial DNA. Structural modeling revealed an overrepresentation of N-mt substitutions at positions that directly contact mutated residues in mitochondrial-encoded proteins, despite overall patterns of conservative structural evolution. These findings support the hypothesis that selection for compensatory changes in response to mitochondrial mutations contributes to the elevated rate of evolution in N-mt genes. We discuss these results in light of theories implicating mitochondrial mutation rates and mitonuclear coevolution as drivers of speciation and suggest comparative and experimental approaches that could take advantage of heterogeneity in rates of mtDNA evolution across eukaryotes to evaluate such theories.
authors.affiliation: Department of Biology, Colorado State University, Fort Collins, Colorado, 80523. justin.havird@colostate.edu.
authors.forename: Justin C
authors.initials: JC
authors.lastname: Havird
authors.affiliation: Department of Computer Science, Colorado State University, Fort Collins, Colorado, 80523.
authors.forename: Nicholas S
authors.initials: NS
authors.lastname: Whitehill
authors.affiliation: Department of Chemical and Biological Engineering, Colorado State University, Fort Collins, Colorado, 80523.
authors.forename: Christopher D
authors.initials: CD
authors.lastname: Snow
authors.affiliation: Department of Biology, Colorado State University, Fort Collins, Colorado, 80523. dan.sloan@colostate.edu.
authors.forename: Daniel B
authors.initials: DB
authors.lastname: Sloan
mesh_terms: D019143:Evolution, Molecular; D054629:Genome, Mitochondrial; D018745:Genome, Plant; D024101:Mitochondrial Proteins / Q000235:genetics* / Q000378:metabolism; D059645:Mutation Rate; D010085:Oxidative Phosphorylation; D017422:Sequence Analysis, DNA; D029751:Silene / Q000235:genetics* / Q000378:metabolism
chemical_list: D024101:Mitochondrial Proteins
keywords: Cytonuclear; electron transport; evolutionary genomics; mitochondrial mutations; mitonuclear interactions