Plastid–Nuclear Interaction and Accelerated Coevolution in Plastid Ribosomal Genes in Geraniaceae

Abstract

Plastids and mitochondria have many protein complexes that include subunits encoded by organelle and nuclear genomes. In animal cells, compensatory evolution between mitochondrial and nuclear-encoded subunits was identified and the high mitochondrial mutation rates were hypothesized to drive compensatory evolution in nuclear genomes. In plant cells, compensatory evolution between plastid and nucleus has rarely been investigated in a phylogenetic framework. To investigate plastid–nuclear coevolution, we focused on plastid ribosomal protein genes that are encoded by plastid and nuclear genomes from 27 Geraniales species. Substitution rates were compared for five sets of genes representing plastid- and nuclear-encoded ribosomal subunit proteins targeted to the cytosol or the plastid as well as nonribosomal protein controls. We found that nonsynonymous substitution rates (dN) and the ratios of nonsynonymous to synonymous substitution rates (ω) were accelerated in both plastid- (CpRP) and nuclear-encoded subunits (NuCpRP) of the plastid ribosome relative to control sequences. Our analyses revealed strong signals of cytonuclear coevolution between plastid- and nuclear-encoded subunits, in which nonsynonymous substitutions in CpRP and NuCpRP tend to occur along the same branches in the Geraniaceae phylogeny. This coevolution pattern cannot be explained by physical interaction between amino acid residues. The forces driving accelerated coevolution varied with cellular compartment of the sequence. Increased ω in CpRP was mainly due to intensified positive selection whereas increased ω in NuCpRP was caused by relaxed purifying selection. In addition, the many indels identified in plastid rRNA genes in Geraniaceae may have contributed to changes in plastid subunits.

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…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.…”

“…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).…”

Expansion of inverted repeat does not decrease substitution rates in Pelargonium plastid genomes

“…2). Because plastid ribosomal protein genes showed accelerated dS in Pelargonium (Guisinger et al, 2008;Weng et al, 2016) and 12 of 15 consensus IR genes were ribosomal protein genes (Table 1), the observation of high substitution rates in the IR is clearly biased by which functional gene group is compared. Indeed, when ribosomal protein genes were excluded, the IR genes showed significantly lower dS than SC genes ( Fig.…”

“…Similarly, locus‐specific rate accelerations were observed for ribosomal protein genes, clpP , ycf1 and ycf2 in Silene (Erixon & Oxelman, ; Sloan et al ., , ). In Geraniaceae, locus‐specific acceleration in both synonymous and nonsynonymous substitution rates were found in ribosomal protein genes and RNA polymerase genes (Guisinger et al ., ; Zhang et al ., ; Weng et al ., ), whereas lineage‐specific rate accelerations were documented in Pelargonium (Weng et al ., ) and Erodium (Blazier et al ., ).…”

Correlated evolution of large DNA fragments in the 3D genome of Arabidopsis thaliana

“…For example, accelerated rates of evolution in nuclear genes that cooperate with mitochondrial genes 4 have been reported in many animal species (Osada and Akashi 2012;Barreto and Burton 2013;Parmakelis et al 2013; Barreto et al 2018), possibly as a result of the high mutation rate in the mitochondrial genome and the accumulation of compensatory mutations in the nuclear genes (Rand et al 2004;Levin et al 2014;Sloan et al 2018). Such accelerated compensatory coevolution has been observed in some plants with elevated mutation rates in the plastid genome as well Weng et al 2016). The correlation of evolutionary rates between interacting genes is evident even at the whole-interactome level in an organism (Fraser et al 2002;Alvarez-Ponce and Fares 2012).…”