Coordinated Rates of Evolution between Interacting Plastid and Nuclear Genes in Geraniaceae

Abstract

Although gene coevolution has been widely observed within individuals and between different organisms, rarely has this phenomenon been investigated within a phylogenetic framework. The Geraniaceae is an attractive system in which to study plastid-nuclear genome coevolution due to the highly elevated evolutionary rates in plastid genomes. In plants, the plastidencoded RNA polymerase (PEP) is a protein complex composed of subunits encoded by both plastid (rpoA, rpoB, rpoC1, and rpoC2) and nuclear genes (sig1-6). We used transcriptome and genomic data for 27 species of Geraniales in a systematic evaluation of coevolution between genes encoding subunits of the PEP holoenzyme. We detected strong correlations of dN (nonsynonymous substitutions) but not dS (synonymous substitutions) within rpoB/sig1 and rpoC2/sig2, but not for other plastid/nuclear gene pairs, and identified the correlation of dN/dS ratio between rpoB/C1/C2 and sig1/5/6, rpoC1/C2 and sig2, and rpoB/C2 and sig3 genes. Correlated rates between interacting plastid and nuclear sequences across the Geraniales could result from plastid-nuclear genome coevolution. Analyses of coevolved amino acid positions suggest that structurally mediated coevolution is not the major driver of plastid-nuclear coevolution. The detection of strong correlation of evolutionary rates between SIG and RNAP genes suggests a plausible explanation for plastome-genome incompatibility in Geraniaceae.

Thermal plasticity of the circadian clock is under nuclear and cytoplasmic control in wild barley

“…Notably, one of the identified nonsynonymous mutations resides within the rpoC1 gene, which is part of the plastid‐encoded RNA polymerase (PEP) protein complex. It is composed of both plastid subunits ( rpoA , rpoB , rpoC1 , and rpoC2 ) and nuclear sigma factors (sig 1‐6); coordinated rates of molecular evolution between the chloroplast and nuclear encoded genes were observed, at least in Geraniaceae (Zhang, Ruhlman, Sabir, Blazier, & Jansen, ). PEP itself has a broad effect on the plastid transcriptome and was already shown to be involved in circadian control.…”

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

“…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 ., ).…”

Loss of aTrans-Splicingnad1Intron from Geraniaceae and Transfer of the Maturase GenematRto the Nucleus inPelargonium

“…In some other species of Viscum (Petersen et al 2015; Skippington et al 2015) and two species within Malpighiales (Wurdack and Davis 2009), the matR gene appears to be missing completely from the mitochondrial genome. Using the extensive genomic and transcriptomic data available for many species within Geraniaceae (Weng et al 2014; Park et al 2015; Zhang et al 2015; Blazier et al 2016), we assessed the status of matR and nad1 in this family and present an evolutionary scenario to explain the unusual structural and functional diversity among species.…”