A Novel Snf2 Protein Maintains trans-Generational Regulatory States Established by Paramutation in Maize

Abstract

Paramutations represent heritable epigenetic alterations that cause departures from Mendelian inheritance. While the mechanism responsible is largely unknown, recent results in both mouse and maize suggest paramutations are correlated with RNA molecules capable of affecting changes in gene expression patterns. In maize, multiple required to maintain repression (rmr) loci stabilize these paramutant states. Here we show rmr1 encodes a novel Snf2 protein that affects both small RNA accumulation and cytosine methylation of a proximal transposon fragment at the Pl1-Rhoades allele. However, these cytosine methylation differences do not define the various epigenetic states associated with paramutations. Pedigree analyses also show RMR1 does not mediate the allelic interactions that typically establish paramutations. Strikingly, our mutant analyses show that Pl1-Rhoades RNA transcript levels are altered independently of transcription rates, implicating a post-transcriptional level of RMR1 action. These results suggest the RNA component of maize paramutation maintains small heterochromatic-like domains that can affect, via the activity of a Snf2 protein, the stability of nascent transcripts from adjacent genes by way of a cotranscriptional repression process. These findings highlight a mechanism by which alleles of endogenous loci can acquire novel expression patterns that are meiotically transmissible.

Maize RNA Polymerase IV Definestrans-Generational Epigenetic Variation

“…Because the Pl1-Rhoades promoter-proximal doppia is a presumed target of Pol IV-facilitated RdDM (Hale et al, 2007), we asked whether loss of doppia cytosine methylation correlated Pl-Rh/Pl-Rh Pl9 /T pl1-R30 +/+ 2 0 0 7…”

Nascent Transcription Affected by RNA Polymerase IV inZea mays

“…The developmental defects observed in rpd1 mutants are both distinct and nonheritable (Parkinson et al 2007) and therefore unlikely to be related to TE-derived mutations. These defects also appear unrelated to siRNA-induced silencing because other maize mutants affecting siRNA biogenesis, including rpd/e2a, are developmentally normal (Hale et al 2007;Stonaker et al 2009;Barbour et al 2012). We hypothesize that maize has co-opted RPD1/Pol IV to transcriptionally control specific alleles of genes for which TEs and TE-like repeats act as regulatory elements.…”

The Pea (Pisum sativum L.) Rogue Paramutation is Accompanied by Alterations in the Methylation Pattern of Specific Genomic Sequences

“…Among the above mentioned maize loci, the most significant progresses have been achieved in the study of b1 and pl1 and the identified genes required for paramutation at these two loci: mediator of paramutation (mop1 [9] and mop2 [10]) and required to maintain repression (rmr1 [11], rmr2 [12], rmr6 [13], and rmr7 [14]) were found to encode proteins involved in small interfering RNA (siRNA) biogenesis and RNA directed DNA methylation (RdDM).…”