Kingdom-wide evolutionary characterization of RNA editing factors across Archaeplastida

RNA editing, a post-transcriptional modification in plant mitochondria and plastids, is essential for environmental adaptation and diverse physiological processes. Despite extensive identification of RNA editing factors, primarily including pentatricopeptide repeat (PPR), multiple organelle RNA editing factor (MORF), organelle RNA recognition motif-containing (ORRM), and organelle zinc finger (OZ) proteins, their evolutionary history remains poorly understood. Here, we perform kingdom-wide evolutionary analyses across 364 high-quality Archaeplastida genomes and find massive PPR gene expansions in early-diverging land plants, predominantly driven by dispersed duplication associated with retroposition. Furthermore, integrative analyses indicate that DYW subgroup PPR genes have been horizontally transferred from plants to bdelloid rotifers, potentially enhancing the recipients’ adaptation to ultraviolet radiation. MORF proteins, accessory partners of PPRs, possess MORF hallmark domains structurally similar to protein-folding peptidase S8 propeptide/proteinase inhibitor I9 domains, suggesting a role in protein folding during RNA editing. Considering diverse domain compositions, we reclassify MORF, ORRM, and OZ proteins and uncover prevalent hallmark domain fusions. Together, these findings illuminate the kingdom-wide evolution of plant RNA editing machinery.