Rickettsial DNA invasions and a scrambled rRNA cluster with a trans-splicing group I intron. : The highly unorthodox mitogenome of the fern Haplopteris ensiformis

Plant chloroplast genomes are conveniently assembled from next generation sequence (NGS) data given their conserved structure and stoichiometric dominance in plant tissues. In contrast, vascular plant mitochondrial genomes are much more complex for assembly given their lack of gene syntenies, their highly recombinogenic structures and the invasion of chloroplast and nuclear or even foreign DNA by horizontal gene transfer (HGT). Leptosporangiate ferns remained the last major clade of land plants for which no mitochondrial genome has been assembled, likely owing to a combination of the above facts. We here present the chloroplast and mitochondrial genomes of a first leptosporangiate fern, Haplopteris ensiformis (Pteridaceae, Polypodiales). Expectedly, the H. ensiformis cpDNA is highly conserved in structure, but we assembled a highly unorthodox and complex mtDNA with numerous repeats separating single-copy regions. Nevertheless, the Haplopteris mtDNA has a rich gene complement lacking only the ccm gene suite. Importantly, it features several sequences indicative of bacterial HGT, mainly from Rickettiales, but also including tRNA genes of chlamydial origin. A particularly complex structure is found for the rrn26 gene which is split in two parts to be reassembled on transcript level by a trans-splicing group I intron. More than 950 events of C-to-U RNA editing and nearly 500 events of reverse U-to-C edits are needed for the maturation of the organelle transcriptomes of Haplopteris ensiformis.