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 plastidnuclear 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.

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

“…2014), OXPHOS complex II proteins (Havird et al. 2015b), or a random set of 50 proteins not targeted to mitochondria or plastids (Rockenbach et al. 2016).…”

“…Although increased d N / d S in N-mt genes could be caused by a change in selection on overall mt function, normal d N / d S values in SDH and mt CLP genes make this unlikely (Havird et al. 2015b; Rockenbach et al. 2016).…”

“…For S. macrodonta , S. latifolia , S. paradoxa , S. noctiflora , S. vulgaris , and the outgroup Agrostemma githago (Fig. 1), we used previously described sequence resources (Rockenbach et al. 2016), based on assembled sets of contigs generated de novo using Trinity r20140717.…”

“…2014; Havird et al. 2015b; Rockenbach et al. 2016), our methods here were slightly different than in previous studies (e.g., different taxa, concatenation schemes, or models in PAML were used), so we reanalyzed these datasets so they would all be processed with the exact same methods.…”

Herbarium genomics: skimming and plastomics from archival specimens

“…However, at the plant species-level plastome exons can be remarkably conserved (or even non-variant) causing sequence alignments to be non-informative. In addition, exon coding regions can be prone to selective and functional constraints that could cause a functional rather than historic signal to be tracked (Ma et al 2014;Rockenbach et al 2016), something to which non-coding regions will not be susceptible. Therefore, aiming for as complete as possible plastomes in genome-skimming phylogenetic projects will pay-off in the longer term.…”