Evolution of highly divergent organellar genomes in two distantly related angiosperm lineages, Eleocharis (Cyperaceae) and papilionoid legumes (Fabaceae)

The plastid genomes (plastomes) of most photosynthetic angiosperms are highly conserved in gene content and order in a gene dense unit-genome. Despite low levels of variation across angiosperms, plastomes of several distantly related lineages experienced a dramatic evolutionary history, including extensive genomic rearrangements, gene duplications and losses, repeat accumulation and expansion and contraction of the inverted repeat (IR). Recently, alternative plastome structures were suggested in the angiosperms, Geraniaceae and Medicago. Here plastomes of two Eleocharis species were completed and revealed remarkably divergent features, including large sizes, high rates of sequence rearrangements, low GC content and gene density, gene duplications and losses, and increased repeat content. A novel finding among these aberrant features was the unprecedented level of heteroplasmy with the presence of multiple plastome structural types within a single individual. To better understand structural evolution on a broader phylogenetic scale, plastomes of 31 legumes in the largest subfamily Papilionoideae, along with three non-papilionoideae were completed and combined with 33 publicly available sequences. A number of IR-related and repeat-mediated changes were identified. Like Eleocharis, intraindividual plastome heteroplasmy associated with ycf2 repeats was confirmed in at least four taxa, which is likely present in most 50 kb-inversion clade. Although loss of the inverted repeat has not been reported in legumes outside of the inverted repeat lacking clade (IRLC), one genistoid taxon was found to completely lack the canonical plastome IR. Correlations between plastome rearrangements and substitution rates have been detected in several angiosperms and mitochondrial and plastid genomes tend to evolve in parallel. Given the fact that Eleocharis plastomes were highly rearranged, sequence evolution of Eleocharis organellar genomes was examined by comparing nucleotide substitution rates within and between plastid and mitochondrial genomes in Eleocharis using 31 Eleocharis species and two other Cyperaceae genera. Mitochondrial sequence evolution of Cyperaceae was also investigated with comparison to other angiosperms. Eleocharis experienced extensive gene losses in both genomes and mitochondrial-specific losses of introns. Correlated lineage- and gene-specific accelerations in dN and dS values were identified in both genomes of Eleocharis. Several clades showed higher dS and dN in mitochondrial genes than plastid genes. In addition, the branch leading to Cyperaceae exhibited dramatically elevated substitution rates compared to most angiosperms. Mitochondrial genes of Cyperaceae exhibited dramatic loss of RNA editing sites and a negative correlation between RNA editing and dS values was detected among angiosperms. Therefore, multiple underlying mechanisms for significant rate accelerations in Eleocharis and Cyperaceae are discussed