Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop

Mol Cell. 2014 Aug 7;55(3):383-96. doi: 10.1016/j.molcel.2014.06.011. Epub 2014 Jul 10.

Abstract

The eukaryotic epigenome is shaped by the genome topology in three-dimensional space. Dynamic reversible variations in this epigenome structure directly influence the transcriptional responses to developmental cues. Here, we show that the Arabidopsis long intergenic noncoding RNA (lincRNA) APOLO is transcribed by RNA polymerases II and V in response to auxin, a phytohormone controlling numerous facets of plant development. This dual APOLO transcription regulates the formation of a chromatin loop encompassing the promoter of its neighboring gene PID, a key regulator of polar auxin transport. Altering APOLO expression affects chromatin loop formation, whereas RNA-dependent DNA methylation, active DNA demethylation, and Polycomb complexes control loop dynamics. This dynamic chromatin topology determines PID expression patterns. Hence, the dual transcription of a lincRNA influences local chromatin topology and directs dynamic auxin-controlled developmental outputs on neighboring genes. This mechanism likely underscores the adaptive success of plants in diverse environments and may be widespread in eukaryotes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chromatin Assembly and Disassembly
  • DNA Methylation
  • DNA-Directed RNA Polymerases / metabolism*
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant
  • Genome, Plant
  • Indoleacetic Acids / pharmacology*
  • Mutation
  • Plant Growth Regulators / pharmacology*
  • Polycomb-Group Proteins / metabolism
  • Protein-Serine-Threonine Kinases / genetics
  • Protein-Serine-Threonine Kinases / metabolism
  • RNA Polymerase II / metabolism*
  • RNA, Long Noncoding / genetics*
  • RNA, Plant / genetics*

Substances

  • Arabidopsis Proteins
  • Indoleacetic Acids
  • Plant Growth Regulators
  • Polycomb-Group Proteins
  • RNA, Long Noncoding
  • RNA, Plant
  • PINOID protein, Arabidopsis
  • Protein-Serine-Threonine Kinases
  • RNA Polymerase II
  • RNA polymerase V, Arabidopsis
  • DNA-Directed RNA Polymerases