Antagonistic Actions of FPA and IBM2 Regulate Transcript Processing from Genes Containing Heterochromatin

Plant Physiol. 2019 May;180(1):392-403. doi: 10.1104/pp.18.01106. Epub 2019 Feb 27.

Abstract

Repressive epigenetic marks, such as DNA and histone methylation, are sometimes located within introns. In Arabidopsis (Arabidopsis thaliana), INCREASE IN BONSAI METHYLATION2 (IBM2), an RNA-binding protein containing a bromo-adjacent homology domain, is required to process functional transcript isoforms of genes carrying intronic heterochromatin. In a genetic screen for suppressors of the ibm2 mutation, we identified FPA, an RNA-binding protein that promotes use of proximal polyadenylation sites in genes targeted by IBM2, including IBM1 encoding an essential H3K9 histone demethylase and the disease resistance gene RECOGNITION OF PERONOSPORA PARASITICA7 Both IBM2 and FPA are involved in the processing of their common mRNA targets: Transcription of IBM2 target genes is restored when FPA is mutated in ibm2 and impaired in transgenic plants overexpressing FPA By contrast, transposons targeted by IBM2 and localized outside introns are not under this antagonistic control. The DNA methylation patterns of some genes and transposons are modified in fpa plants, including the large intron of IBM1, but these changes are rather limited and reversed when the mutant is complemented, indicating that FPA has a restricted role in mediating silencing. These data reveal a complex regulation by IBM2 and FPA pathways in processing mRNAs of genes bearing heterochromatic marks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • DNA Methylation
  • DNA Transposable Elements
  • Gene Expression Regulation, Plant*
  • Genes, Suppressor
  • Heterochromatin / genetics*
  • Introns
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Mutation
  • Plants, Genetically Modified
  • Polyadenylation
  • RNA, Messenger / genetics
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*

Substances

  • Arabidopsis Proteins
  • DNA Transposable Elements
  • FPA protein, Arabidopsis
  • Heterochromatin
  • RNA, Messenger
  • RNA-Binding Proteins
  • RPP7 protein, Arabidopsis
  • IBM1 protein, Arabidopsis
  • IBM2 protein, Arabidopsis
  • Jumonji Domain-Containing Histone Demethylases