title: The Roles of Compensatory Evolution and Constraint in Aminoacyl tRNA Synthetase Evolution.
abstract: Mitochondrial protein translation requires interactions between transfer RNAs encoded by the mitochondrial genome (mt-tRNAs) and mitochondrial aminoacyl tRNA synthetase proteins (mt-aaRS) encoded by the nuclear genome. It has been argued that animal mt-tRNAs have higher deleterious substitution rates relative to their nuclear-encoded counterparts, the cytoplasmic tRNAs (cyt-tRNAs). This dynamic predicts elevated rates of compensatory evolution of mt-aaRS that interact with mt-tRNAs, relative to aaRS that interact with cyt-tRNAs (cyt-aaRS). We find that mt-aaRS do evolve at significantly higher rates (exemplified by higher dN and dN/dS) relative to cyt-aaRS, across mammals, birds, and Drosophila. While this pattern supports a model of compensatory evolution, the level at which a gene is expressed is a more general predictor of protein evolutionary rate. We find that gene expression level explains 10-56% of the variance in aaRS dN/dS, and that cyt-aaRS are more highly expressed in addition to having lower dN/dS values relative to mt-aaRS, consistent with more highly expressed genes being more evolutionarily constrained. Furthermore, we find no evidence of positive selection acting on either class of aaRS protein, as would be expected under a model of compensatory evolution. Nevertheless, the signature of faster mt-aaRS evolution persists in mammalian, but not bird or Drosophila, lineages after controlling for gene expression, suggesting some additional effect of compensatory evolution for mammalian mt-aaRS. We conclude that gene expression is the strongest factor governing differential amino acid substitution rates in proteins interacting with mitochondrial versus cytoplasmic factors, with important differences in mt-aaRS molecular evolution among taxonomic groups.
authors.affiliation: Department of Biology, Indiana University, Bloomington.
authors.forename: Jeffrey R
authors.initials: JR
authors.lastname: Adrion
authors.affiliation: Department of Biology, Indiana University, Bloomington.
authors.forename: P Signe
authors.initials: PS
authors.lastname: White
authors.affiliation: Department of Biology, Indiana University, Bloomington kmontooth2@unl.edu.
authors.forename: Kristi L
authors.initials: KL
authors.lastname: Montooth
mesh_terms: D000604:Amino Acyl-tRNA Synthetases / Q000235:genetics*; D000818:Animals; D001717:Birds / Q000235:genetics; D002467:Cell Nucleus / Q000235:genetics; D004330:Drosophila / Q000235:genetics; D019143:Evolution, Molecular; D015870:Gene Expression / Q000235:genetics*; D054629:Genome, Mitochondrial / Q000235:genetics*; D006801:Humans; D008928:Mitochondria / Q000235:genetics
chemical_list: D000604:Amino Acyl-tRNA Synthetases
keywords: compensatory evolution; gene expression; mitochondrial-nuclear coevolution; protein evolution