Overlapping RdDM and non-RdDM mechanisms work together to maintain somatic repression of a paramutagenic epiallele of maize pericarp color1

PLoS One. 2017 Nov 7;12(11):e0187157. doi: 10.1371/journal.pone.0187157. eCollection 2017.

Abstract

Allelic variation at the Zea mays (maize) pericarp color1 (p1) gene has been attributed to epigenetic gene regulation. A p1 distal enhancer, 5.2 kb upstream of the transcriptional start site, has demonstrated variation in DNA methylation in different p1 alleles/epialleles. In addition, DNA methylation of sequences within the 3' end of intron 2 also plays a role in tissue-specific expression of p1 alleles. We show here a direct evidence for small RNAs' involvement in regulating p1 that has not been demonstrated previously. The role of mediator of paramutation1 (mop1) was tested in the maintenance of somatic silencing at distinct p1 alleles: the non-paramutagenic P1-wr allele and paramutagenic P1-rr' epiallele. The mop1-1 mutation gradually relieves the silenced phenotype after multiple generations of exposure; P1-wr;mop1-1 plants display a loss of 24-nt small RNAs and DNA methylation in the 3' end of the intron 2, a region close to a Stowaway transposon. In addition, a MULE sequence within the proximal promoter of P1-wr shows depletion of 24nt siRNAs in mop1-1 plants. Release of silencing was not correlated with small RNAs at the distal enhancer region of the P1-wr allele. We found that the somatic silencing of the paramutagenic P1-rr' is correlated with significantly reduced H3K9me2 in the distal enhancer of P1-rr'; mop1-1 plants, while symmetric DNA methylation is not significantly different. This study highlights that the epigenetic regulation of p1 alleles is controlled both via RdDM as well as non-RdDM mechanisms.

MeSH terms

  • Alleles*
  • DNA Methylation
  • Enhancer Elements, Genetic
  • Epigenesis, Genetic
  • Gene Silencing
  • Genes, Plant
  • Introns
  • Mutagens*
  • Zea mays / genetics*

Substances

  • Mutagens

Grants and funding

This work was supported by National Science Foundation collaborative awards 0619330 and 1051654 to SC and 1051576 to BCM. Support from Hatch awards PEN04452 and PEN04613 to SC is acknowledged. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.