Kingdom-wide evolutionary characterization of RNA editing factors in Archaeplastida

RNA editing, a post-transcriptional modification in plant mitochondria and plastids, is essential for plant terrestrialization. Editosome, mediating RNA editing, comprises nuclear-encoded factors, primarily including pentatricopeptide repeat (PPR), multiple organelle RNA editing factor (MORF), organelle RNA recognition motif-containing (ORRM), and organelle zinc finger (OZ) proteins. However, the origin, evolution, and diversification of these editing factors largely remain enigmatic. Here, we analyze 364 high-quality proteomes spanning Archaeplastida to identify 212,779 PPR, 2,759 MORF, 7,760 ORRM and 829 OZ proteins, and chart their evolutionary landscapes. We find that PPR genes in terrestrial plants undergo substantial expansions, mainly driven by dispersed duplication and retroposition. Further analysis shows that DYW subgroup PPR genes, encoding RNA-editing enzymes, are largely transferred from plants to rotifers, potentially enhancing ultraviolet irradiation resistance of these recipients. Meanwhile, we find that MORF proteins, accessory factors of PPR proteins, are restricted to seed plants. Notably, their hallmark MORF domains share sequence and structural similarity with peptidase S8 propeptide/proteinase inhibitor I9 domains that mediate pro-enzyme folding, implying MORFs regulate PPR folding. Additionally, we reclassify MORF, ORRM, and OZ proteins based on domain architecture, revealing hallmark domain fusions occur among them and with PPR proteins, except between MORF and OZ. Collectively, our findings shed light on the evolution of plant RNA editing factors.