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Paramutation involves homologous sequence communication that leads to meiotically heritable transcriptional silencing. We demonstrate that  mop2  ( mediator of paramutation2 ), which alters paramutation at multiple loci, encodes a gene similar to Arabidopsis NRPD2/E2, the second-largest subunit of plant-specific RNA polymerases IV and V. In Arabidopsis, Pol-IV and Pol-V play major roles in RNA–mediated silencing and a single second-largest subunit is shared between Pol-IV and Pol-V. Maize encodes three second-largest subunit genes: all three genes potentially encode full length proteins with highly conserved polymerase domains, and each are expressed in multiple overlapping tissues. The isolation of a recessive paramutation mutation in  mop2  from a forward genetic screen suggests limited or no functional redundancy of these three genes. Potential alternative Pol-IV/Pol-V–like complexes could provide maize with a greater diversification of RNA–mediated transcriptional silencing machinery relative to Arabidopsis.  Mop2-1  disrupts paramutation at multiple loci when heterozygous, whereas previously silenced alleles are only up-regulated when  Mop2-1  is homozygous. The dramatic reduction in  b1  tandem repeat siRNAs, but no disruption of silencing in  Mop2-1  heterozygotes, suggests the major role for tandem repeat siRNAs is not to maintain silencing. Instead, we hypothesize the tandem repeat siRNAs mediate the establishment of the heritable silent state—a process fully disrupted in  Mop2-1  heterozygotes. The dominant  Mop2-1  mutation, which has a single nucleotide change in a domain highly conserved among all polymerases ( E. coli  to eukaryotes), disrupts both siRNA biogenesis (Pol-IV–like) and potentially processes downstream (Pol-V–like). These results suggest either the wild-type protein is a subunit in both complexes or the dominant mutant protein disrupts both complexes. Dominant mutations in the same domain in  E. coli  RNA polymerase suggest a model for  Mop2-1  dominance: complexes containing  Mop2-1  subunits are non-functional and compete with wild-type complexes.

plos genetics

A Dominant Mutation in mediator of paramutation2, One of Three Second-Largest Subunits of a Plant-Specific RNA Polymerase, Disrupts Multiple siRNA Silencing Processes