Extensive variation in nucleotide substitution rate and gene/intron loss in mitochondrial genomes of Pelargonium

Abstract

Geraniaceae organelle genomes have been shown to exhibit several highly unusual features compared to most other photosynthetic angiosperms. This includes massively rearranged plastomes with considerable size variation, extensive gene and intron loss, accelerated rates of nucleotide substitutions in both mitogenomes and plastomes, and biparental inheritance and cytonuclear incompatibility of the plastome. Most previous studies have focused on plastome evolution with mitogenome comparisons limited to only a few taxa or genes. In this study, mitogenomes and transcriptomes were examined for 27 species of Geraniales, including 13 species of Pelargonium. Extensive gene and intron losses were detected across the Geraniales with Pelargonium representing the most gene depauperate lineage in the family. Plotting these events on the Geraniaceae phylogenetic tree showed that gene losses occurred multiple times, whereas intron losses more closely reflected the relationships among taxa. In addition, P. australe acquired an intron by horizontal transfer. Comparisons of nucleotide substitution rates in Pelargonium showed that synonymous changes in nuclear genes were much lower than in mitochondrial genes. This is in contrast to the previously published studies that indicated that nuclear genes have 16 fold higher rates than mitochondrial genes across angiosperms. Elevated synonymous substitutions occurred for each mitochondrial gene in Pelargonium with the highest values 783 and 324 times higher than outgroups and other Geraniaceae, respectively. Pelargonium is one of four unrelated genera of angiosperms (Ajuga, Plantago and Silene) that have experienced highly accelerated nucleotide substitutions in mitogenomes. It is distinct from most angiosperms in also having elevated substitution rates in plastid genes but the cause of rate accelerations in Pelargonium plastomes and mitogenomes may be different.

Keywords: Gene loss; Geraniaceae; Intron loss; Mitogenome; Pelargonium; Substitution rate.