title: Positive Selection in Rapidly Evolving Plastid-Nuclear Enzyme Complexes.
abstract: Rates of sequence evolution in plastid genomes are generally low, but numerous angiosperm lineages exhibit accelerated evolutionary rates in similar subsets of plastid genes. These genes include clpP1 and accD, which encode components of the caseinolytic protease (CLP) and acetyl-coA carboxylase (ACCase) complexes, respectively. Whether these extreme and repeated accelerations in rates of plastid genome evolution result from adaptive change in proteins (i.e., positive selection) or simply a loss of functional constraint (i.e., relaxed purifying selection) is a source of ongoing controversy. To address this, we have taken advantage of the multiple independent accelerations that have occurred within the genus Silene (Caryophyllaceae) by examining phylogenetic and population genetic variation in the nuclear genes that encode subunits of the CLP and ACCase complexes. We found that, in species with accelerated plastid genome evolution, the nuclear-encoded subunits in the CLP and ACCase complexes are also evolving rapidly, especially those involved in direct physical interactions with plastid-encoded proteins. A massive excess of nonsynonymous substitutions between species relative to levels of intraspecific polymorphism indicated a history of strong positive selection (particularly in CLP genes). Interestingly, however, some species are likely undergoing loss of the native (heteromeric) plastid ACCase and putative functional replacement by a duplicated cytosolic (homomeric) ACCase. Overall, the patterns of molecular evolution in these plastid-nuclear complexes are unusual for anciently conserved enzymes. They instead resemble cases of antagonistic coevolution between pathogens and host immune genes. We discuss a possible role of plastid-nuclear conflict as a novel cause of accelerated evolution.
authors.affiliation: Department of Biology, Colorado State University, Fort Collins, Colorado 80523.
authors.forename: Kate
authors.initials: K
authors.lastname: Rockenbach
authors.affiliation: Department of Biology, Colorado State University, Fort Collins, Colorado 80523.
authors.forename: Justin C
authors.initials: JC
authors.lastname: Havird
authors.affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, Colorado 80523.
authors.forename: J Grey
authors.initials: JG
authors.lastname: Monroe
authors.affiliation: Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611.
authors.forename: Deborah A
authors.initials: DA
authors.lastname: Triant
authors.affiliation: Department of Biology, University of Virginia, Charlottesville, Virginia 22904.
authors.forename: Douglas R
authors.initials: DR
authors.lastname: Taylor
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: D000103:Acetyl-CoA Carboxylase / Q000235:genetics*; D060365:Chloroplast Proteins / Q000235:genetics*; D049071:Endopeptidase Clp / Q000235:genetics*; D019143:Evolution, Molecular; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics*; D011110:Polymorphism, Genetic; D012641:Selection, Genetic; D029751:Silene / Q000145:classification / Q000235:genetics* / Q000378:metabolism
chemical_list: D060365:Chloroplast Proteins; D010940:Plant Proteins; D049071:Endopeptidase Clp; D000103:Acetyl-CoA Carboxylase
keywords: McDonald–Kreitman test; chloroplast; cytonuclear interactions; plastome