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To understand the molecular mechanisms underlying paramutation, we examined the role of  Unstable factor for orange1  ( Ufo1 ) in maintaining paramutation at the maize  pericarp color1  ( p1 ) and  booster1  ( b1 ) loci. Genetic tests revealed that the  Ufo1-1  mutation disrupted silencing associated with paramutation at both  p1  and  b1 . The level of up regulation achieved at  b1  was lower than that at  p1 , suggesting differences in the role  Ufo1-1  plays at these loci. We characterized the interaction of  Ufo1-1  with two silenced  p1  epialleles,  P1-rr ′ and  P1-pr TP  , that were derived from a common  P1-rr  ancestor. Both alleles are phenotypically indistinguishable, but differ in their paramutagenic activity;  P1-rr′  is paramutagenic to  P1-rr , while  P1-pr TP   is non-paramutagenic. Analysis of cytosine methylation revealed striking differences within an enhancer fragment that is required for paramutation;  P1-rr ′ exhibited increased methylation at symmetric (CG and CHG) and asymmetric (CHH) sites, while  P1-pr TP   was methylated only at symmetric sites. Both silenced alleles had higher levels of dimethylation of lysine 9 on histone 3 (H3K9me2), an epigenetic mark of silent chromatin, in the enhancer region. Both epialleles were reactivated in the  Ufo1-1  background; however, reactivation of  P1-rr′  was associated with dramatic loss of symmetric and asymmetric cytosine methylation in the enhancer, while methylation of up-regulated  P1-pr TP   was not affected. Interestingly,  Ufo1-1 –mediated reactivation of both alleles was accompanied with loss of H3K9me2 mark from the enhancer region. Therefore, while earlier studies have shown correlation between H3K9me2 and DNA methylation, our study shows that these two epigenetic marks are uncoupled in the  Ufo1-1 –reactivated  p1  alleles. Furthermore, while CHH methylation at the enhancer region appears to be the major distinguishing mark between paramutagenic and non-paramutagenic  p1  alleles, H3K9me2 mark appears to be important for maintaining epigenetic silencing.

Maize Unstable factor for orange1 Is Required for Maintaining Silencing Associated with Paramutation at the pericarp color1 and booster1 Loci