Step‐wise and lineage‐specific diversification of plant RNA polymerase genes and origin of the largest plant‐specific subunits

Abstract

SummaryProteins often function as complexes, yet little is known about the evolution of dissimilar subunits of complexes. DNA-directed RNA polymerases (RNAPs) are multisubunit complexes, with distinct eukaryotic types for different classes of transcripts. In addition to Pol I-III, common in eukaryotes, plants have Pol IV and V for epigenetic regulation. Some RNAP subunits are specific to one type, whereas other subunits are shared by multiple types.We have conducted extensive phylogenetic and sequence analyses, and have placed RNAP gene duplication events in land plant history, thereby reconstructing the subunit compositions of the novel RNAPs during land plant evolution.We found that Pol IV/V have experienced step-wise duplication and diversification of various subunits, with increasingly distinctive subunit compositions. Also, lineage-specific duplications have further increased RNAP complexity with distinct copies in different plant families and varying divergence for subunits of different RNAPs. Further, the largest subunits of Pol IV/V probably originated from a gene fusion in the ancestral land plants.We propose a framework of plant RNAP evolution, providing an excellent model for protein complex evolution.

RNA Pol IV and V in gene silencing: Rebel polymerases evolving away from Pol II's rules

“…These polymerases, designated Nuclear RNA Polymerase (NRP) B, D, or E in reference to Pols II, IV, and V, respectively, are comprised of 12 core subunits and approximately half of these subunits are shared by all three polymerases [42,46] (Figure 2). Current data suggests that the unique subunits of Pol IV and Pol V arose from their Pol II counterparts via many independent duplication events, starting prior to the evolution of land plants, followed by “Escape from Adaptive Conflict” sub-functionalization [47–50]. Indeed, contrary to previous reports [47,48], all land plants have specialized Pol IV and Pol V complexes [49,50] with unique catalytic cores and 7 th subunits [48–50].…”

“…Current data suggests that the unique subunits of Pol IV and Pol V arose from their Pol II counterparts via many independent duplication events, starting prior to the evolution of land plants, followed by “Escape from Adaptive Conflict” sub-functionalization [47–50]. Indeed, contrary to previous reports [47,48], all land plants have specialized Pol IV and Pol V complexes [49,50] with unique catalytic cores and 7 th subunits [48–50]. On the other hand, additional 4 th and 5 th subunits appear to be unique to flowering [48–50] and seed plants [49], respectively.…”

Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data

“…These observations led to the suggestion that, unlike phasiRNAs and miRNAs, hc-siRNAs were not universal features found in all land plants (Dolgosheina et al, 2008). However, homologs of key genes known to be responsible for hcsiRNA biogenesis and function in angiosperms clearly exist in diverse plant lineages (Zong et al, 2009;Banks et al, 2011;Huang et al, 2015;Wang and Ma, 2015;You et al, 2017). Reverse genetic analyses of these homologs, coupled with sRNA-seq analyses of the mutants, has shown that hc-siRNAs exist in the moss P. patens (Cho et al, 2008;Coruh et al, 2015), which implies that the pathway was most likely present in the last common ancestor of all land plants.…”

Functional Dissection of the Pol V Largest Subunit CTD in RNA-Directed DNA Methylation

“…Approximately half of the Pol V subunits are encoded by the same genes as Pol II subunits (Ream et al, 2013; Ream et al, 2009). Remaining subunits, including the catalytic subunits (the two largest subunits), are encoded by genes that arose through duplication and sub-functionalization of ancestral Pol II subunit genes (Huang et al, 2015; Luo and Hall, 2007; Ream et al, 2009; Tucker et al, 2010; Wang and Ma, 2015). A major distinguishing feature of Pol V is the largest subunit, NRPE1, which is characterized by a long C-terminal domain (CTD), spanning ~700 amino acids.…”