Cytonuclear Interactions and Relaxed Selection Accelerate Sequence Evolution in Organelle Ribosomes

Abstract

Many mitochondrial and plastid protein complexes contain subunits that are encoded in different genomes. In animals, nuclear-encoded mitochondrial proteins often exhibit rapid sequence evolution, which has been hypothesized to result from selection for mutations that compensate for changes in interacting subunits encoded in mutation-prone animal mitochondrial DNA. To test this hypothesis, we analyzed nuclear genes encoding cytosolic and organelle ribosomal proteins in flowering plants. The model angiosperm genus Arabidopsis exhibits low organelle mutation rates, typical of most plants. Nevertheless, we found that (nuclear-encoded) subunits of organelle ribosomes in Arabidopsis have higher amino acid sequence polymorphism and divergence than their counterparts in cytosolic ribosomes, suggesting that organelle ribosomes experience relaxed functional constraint. However, the observed difference between organelle and cytosolic ribosomes was smaller than in animals and could be partially attributed to rapid evolution in N-terminal organelle-targeting peptides that are not involved in ribosome function. To test the role of organelle mutation more directly, we used transcriptomic data from an angiosperm genus (Silene) with highly variable rates of organelle genome evolution. We found that Silene species with unusually fast-evolving mitochondrial and plastid DNA exhibited increased amino acid sequence divergence in ribosomal proteins targeted to the organelles but not in those that function in cytosolic ribosomes. Overall, these findings support the hypothesis that rapid organelle genome evolution has selected for compensatory mutations in nuclear-encoded proteins. We conclude that coevolution between interacting subunits encoded in different genomic compartments within the eukaryotic cell is an important determinant of variation in rates of protein sequence evolution.

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…First, if a demographic bottleneck had occurred, we would expect an excess of nonsynonymous divergence across all genes, but we did not observe this in the mtCLP genes or the randomly chosen nuclear genes. Previous studies in Silene also support the conclusion that the observed changes are not the result of genome-wide demographic effects; analysis of 140 cytosolic ribosomal proteins and seven mitochondrial-targeted complex II genes in S. conica and S. noctiflora did not show elevated d N /d S relative to other Silene species (Sloan et al 2014b;Havird et al 2015). Second, we observed elevated levels of nonsynonymous divergence across different timescales in our MK tests (Table 3 and Table S7) by using two different outgroups: S. latifolia (5.7 MY divergence time) and S. macrodonta (1.8 MY divergence time; Rautenberg et al 2012).…”

“…In addition, recent studies showed correlated increases in d N /d S 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 d N /d S , positive selection and relaxed purifying selection, which can be difficult to disentangle based on sequence divergence data alone.…”

“…Transcriptomes for these six species (S. conica, S. latifolia, S. noctiflora, S. paradoxa, S. vulgaris, and Ag. githago) were taken from previously described data sets (Sloan et al 2014b) that were each generated from a single individual and assembled with Trinity r20120608 (Grabherr et al 2011). These data sets were used for all phylogenetic analyses and correspond to NCBI Sequence Read Archive (SRA) accessions SRX353031, SRX353047, SRX353048, SRX353049, SRX353050, and SRX352988.…”

“…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).…”

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

“…Indeed, interactions between organellar genomes (mitochondria and plastids) and host genotypes appear to often affect host fitness (e.g., refs. [17][18][19][20].…”