Analyses of charophyte chloroplast genomes help characterize theancestral chloroplastgenomeof land plants

Abstract

Despite the significanceof therelationshipsbetweenembryophytesandtheir charophyte algal ancestors in deciphering theoriginand evolutionary success of land plants, few chloroplast genomes of the charophyte algae have been reconstructed to date. Here, we present new data for three chloroplast genomes of the freshwater charophytes Klebsormidium flaccidum (Klebsormidiophyceae), Mesotaenium endlicherianum (Zygnematophyceae), and Roya anglica (Zygnematophyceae). The chloroplast genome of Klebsormidium has a quadripartite organization with exceptionally large inverted repeat (IR) regions and, uniquely among streptophytes, has lost the rrn5andrrn4.5genes fromthe ribosomalRNA(rRNA)gene clusteroperon.ThechloroplastgenomeofRoya differs from other zygnematophycean chloroplasts, including the newly sequenced Mesotaenium, by having a quadripartite structure that is typicalofother streptophytes. Onthebasis of the improbabilityof the novelgainof IRregions,we infer that thequadripartite structure has likely been lost independently in at least three zygnematophycean lineages, although the absence of the usual rRNA operonic synteny in the IR regions of Roya may indicate their de novo origin. Significantly, all zygnematophycean chloroplast genomes have undergone substantial genomic rearrangement, whichmay be the result of ancient retroelement activity evidenced by the presence of integrase-like and reverse transcriptase-like elements in the Roya chloroplast genome. Our results corroborate the close phylogenetic relationship between Zygnematophyceae and land plants and identify 89 protein-coding genes and 22 introns present in the chloroplastgenome at thetime of the evolutionary transitionofplants toland, allofwhich canbe foundinthe chloroplastgenomesof extant charophytes. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.