Maize RNA polymerase IV defines trans-generational epigenetic variation

Plant Cell. 2013 Mar;25(3):808-19. doi: 10.1105/tpc.112.107680. Epub 2013 Mar 19.

Abstract

The maize (Zea mays) RNA Polymerase IV (Pol IV) largest subunit, RNA Polymerase D1 (RPD1 or NRPD1), is required for facilitating paramutations, restricting expression patterns of genes required for normal development, and generating small interfering RNA (siRNAs). Despite this expanded role for maize Pol IV relative to Arabidopsis thaliana, neither the general characteristics of Pol IV-regulated haplotypes, nor their prevalence, are known. Here, we show that specific haplotypes of the purple plant1 locus, encoding an anthocyanin pigment regulator, acquire and retain an expanded expression domain following transmission from siRNA biogenesis mutants. This conditioned expression pattern is progressively enhanced over generations in Pol IV mutants and then remains heritable after restoration of Pol IV function. This unusual genetic behavior is associated with promoter-proximal transposon fragments but is independent of sequences required for paramutation. These results indicate that trans-generational Pol IV action defines the expression patterns of haplotypes using co-opted transposon-derived sequences as regulatory elements. Our results provide a molecular framework for the concept that induced changes to the heterochromatic component of the genome are coincident with heritable changes in gene regulation. Alterations of this Pol IV-based regulatory system can generate potentially desirable and adaptive traits for selection to act upon.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alleles
  • Anthocyanins / genetics
  • Anthocyanins / metabolism
  • Chromatin Assembly and Disassembly
  • DNA Transposable Elements
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism*
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Plant*
  • Genetic Loci
  • Haplotypes
  • Inheritance Patterns
  • Molecular Sequence Data
  • Phenotype
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • RNA, Plant / genetics
  • RNA, Plant / metabolism*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Regulatory Sequences, Nucleic Acid
  • Selection, Genetic
  • Zea mays / enzymology*
  • Zea mays / genetics*

Substances

  • Anthocyanins
  • DNA Transposable Elements
  • Plant Proteins
  • RNA, Plant
  • RNA, Small Interfering
  • DNA-Directed RNA Polymerases

Associated data

  • GENBANK/JX556412
  • GENBANK/JX556413