Academic journal article Genetics

Positive Selection in Rapidly Evolving Plastid-Nuclear Enzyme Complexes

Academic journal article Genetics

Positive Selection in Rapidly Evolving Plastid-Nuclear Enzyme Complexes

Article excerpt

PLASTIDS carry reduced genomes that reflect an evolutionary history of extensive gene loss and transfer to the nucleus since their ancient endosymbiotic origin roughly 1 billion years ago (Timmis et al. 2004; Keeling 2010; Gray and Archibald 2012). Many of the proteins encoded by genes that have been transferred to the nuclear genome are trafficked back into the plastid (Gould et al. 2008), where they interact closely with proteins encoded by genes remaining in the plastid genome. These interacting proteins are key not only to photosynthesis, but also to transcription, translation, and critical nonphotosynthetic metabolic functions of the plastid. The interactions between these gene products create the opportunity for coevolution between plastid and nuclear genomes. Thus, studying the nuclear genes that contribute to plastid complexes is a valuable tool for understanding the processes underlying plastid genome evolution and cytonuclear coevolution.

Within angiosperms, most plastid genomes are highly conserved in sequence and structure (Jansen et al. 2007; Wicke et al. 2011), but multiple independent lineages have experienced accelerated rates of aa substitution in similar subsets of nonphotosynthetic genes (Jansen et al. 2007; Erixon and Oxelman 2008; Greiner et al. 2008b; Guisinger et al. 2008, 2010, 2011; Straub et al. 2011; Sloan et al. 2012a, 2014a; Barnard-Kubow et al. 2014; Weng et al. 2014; Dugas et al. 2015; Williams et al. 2015; Zhang et al. 2016). Several mechanisms have been hypothesized to explain these repeated accelerations including positive selection, reduced effective population size (Ne), altered DNA repair, changes in gene expression, and pseudogenization following gene transfer to the nucleus (see above citations). Distinguishing among these hypotheses has proved challenging, and the ultimate cause or causes of the extreme differences in rates of molecular evolution among genes within plastid genomes remain unclear.

In many cases of extreme plastid genome evolution, accelerations have disproportionately affected nonsynonymous sites, resulting in elevated ratios of nonsynonymous to synonymous substitution rates (dN/dS) (e.g., Erixon and Oxelman 2008; Guisinger et al. 2008; Barnard-Kubow et al. 2014; Sloan et al. 2014a), which indicates that changes in selection are likely involved. In addition, recent studies showed correlated increases in dN/dS between nuclear- and plastidencoded subunits in ribosomal (Sloan et al. 2014b; Weng et al. 2016) and RNA polymerase complexes (Zhang et al. 2015), providing further evidence for changes in selection pressures. However, these studies could not confidently distinguish between two alternative explanations for increased dN/dS, positive selection and relaxed purifying selection, which can be difficult to disentangle based on sequence divergence data alone. Because these selection pressures can have very different effects on population genetic variation, analyses that combine data on intraspecific polymorphism and interspecific divergence (McDonald and Kreitman 1991) can detect positive selection even in cases where it is not readily identifiable based only on dN/dS (Rausher et al. 2008). However, most studies of accelerated plastid genome evolution and plastid-nuclear coevolution have not included the necessary intraspecific polymorphism data to perform these analyses.

In contrast to recent analyses of plastid genetic machinery (i.e., ribosomal and RNA polymerase genes; Sloan et al. 2014b; Zhang et al. 2015; Weng et al. 2016), the potential for molecular coevolution involving nuclear-encoded subunits in other plastid complexes remains largely unexplored. Two such complexes are the caseinolytic protease (CLP), which is an ATP-dependent protease required for proper plastid function (Nishimura and van Wijk 2015), and the heteromeric acetyl-coA carboxylase (ACCase), which is involved in fatty acid biosynthesis (Sasaki and Nagano 2004; Salie and Thelen 2016). …

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