Dynamics of group II introns in plant mitogenomes and rickettsial DNA invasions in the mitogenome of <em>Haplopteris ensiformis</em>

Abstract

The complexity of mitochondrial genomes (mtDNA) in vascular plants is well-known, with factors such as repetitive sequences, variable structural organization, gene synteny decline, high intron content, and RNA editing contributing to their intricate nature. However, investigations into the mtDNA of ferns belonging to the taxonomically diverse group of polypodiales have been hindered by a combination of these factors. In this study, we discovered that the fern species Haplopteris ensiformis possesses a complex mtDNA with circular chromosomes, trans-splicing of group I introns, and extensive RNA editing. Notably, it also contains DNA from chloroplasts and rickettsial bacteria, through horizontal gene transfer. The assembly of H. ensiformis mtDNA allowed for the study of mitochondrial group II introns in ferns and other land plant lineages. <br> The search for the evolutionary origin of the enigmatic distribution of land plant mitochondrial group II intron revealed evolutionary recent and ancient intron dynamics. Additionally, rare intron configurations, like introns-within-introns (twintrons) and yet undescribed zombie-twintrons, in the vascular plant family of Lycopodiaceae and the bryophyte lineage of hornworts, have been discovered adding yet another layer of complexity of land plant mtDNAs. Through systematic investigation of group II introns and associated proteins, the maturases, we also identified evidence of ancient mobility and coevolution of plant mitochondrial group II introns with nuclear-encoded proteins responsible for organellar splicing. Here, these findings provide insights into the evolutionary interdependency between cytonuclear interactions and mitochondrial intron splicing but raise questions about the mechanistic origin of plant mitogenome intron dynamics.