The Loss-and-Gain Strategy for Functional Specialization of Plant-Specific RNA Polymerases

Plant cells possess functionally specialized RNA polymerases (RNAPs) in both the nucleus and the chloroplast. In addition to the conserved RNA polymerase I (Pol I), Pol II, and Pol III, the nuclear genome of land plant cells encodes two unique multiple-subunit DNA-dependent RNAPs-Pol IV and Pol V-which produce noncoding RNAs for nuclear gene silencing. The plastid genome of all plant cells also encodes a unique multiple-subunit DNA-dependent RNAP-the plastid-encoded RNAP (PEP). Phylogenetic analyses indicate that these plant-specific RNAPs have clear evolutionary origins: Pol IV and Pol V diverged from Pol II, while PEP originated from cyanobacterial RNAP. Over billions of years, these plant-specific RNAPs underwent functional specialization through losing key residues, motifs, and domains essential to their ancestors' function and gaining new motifs, domains, and subunits tailored to their distinct roles. This review explores the evolutionary loss-and-gain strategy that shaped the three plant-specific RNAPs.