Towards a plant model for enigmatic U-to-C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis

Hornworts have a crucial role for understanding the early phylogeny of land plants, as the possible sister clade to vascular plants (tracheophytes). The emergence of “reverse” U-to-C RNA editing to accompany the more widespread C-to-U RNA editing in plant chloroplasts and mitochondria could be a molecular synapomorphy supporting a joint hornwort-tracheophyte (HT) clade. The molecular mechanisms of C-to-U RNA editing are reasonably well understood after identification of many editing factors in models like the flowering plant Arabidopsis thaliana and the moss Physcomitrella patens, but there is no established model system to investigate U-to-C RNA editing, which is abundantly present only in hornworts, lycophytes and ferns. The hornwort Anthoceros agrestis is now emerging as such a plant model. We here report on the assembly and analyses of its chloroplast and mito¬chondrial genomes, transcriptomes and editomes. Among the interesting features of the A. agrestis mtDNA are a high abundance of organelle introns, some of which lack homologues anywhere else in the living world. Both organelles in A. agrestis feature high amounts of RNA editing in both directions of pyrimidine exchange with altogether more than 1,100 sites of C-to-U and more than 1,300 sites of U-to-C editing. The Anthoceros agrestis nuclear genome assemblies reveal over 1,400 genes for “DYW-type” pentatricopeptide repeat (PPR) proteins, like the factors identified for C-to-U editing in the established plant models. Intriguingly, we observe significantly different variants of the DYW domain, the likely cytidine deaminase for C-to-U editing and here discuss the first attractive candidates for reverse U-to-C editing factors given their matches to reverse editing targets according to the PPR-RNA binding code.