The Arabidopsis GAGA-Binding Factor BASIC PENTACYSTEINE6 Recruits the POLYCOMB-REPRESSIVE COMPLEX1 Component LIKE HETEROCHROMATIN PROTEIN1 to GAGA DNA Motifs

Plant Physiol. 2015 Jul;168(3):1013-24. doi: 10.1104/pp.15.00409. Epub 2015 May 29.

Abstract

Polycomb-repressive complexes (PRCs) play key roles in development by repressing a large number of genes involved in various functions. Much, however, remains to be discovered about PRC-silencing mechanisms as well as their targeting to specific genomic regions. Besides other mechanisms, GAGA-binding factors in animals can guide PRC members in a sequence-specific manner to Polycomb-responsive DNA elements. Here, we show that the Arabidopsis (Arabidopsis thaliana) GAGA-motif binding factor protein basic pentacysteine6 (BPC6) interacts with like heterochromatin protein1 (LHP1), a PRC1 component, and associates with vernalization2 (VRN2), a PRC2 component, in vivo. By using a modified DNA-protein interaction enzyme-linked immunosorbant assay, we could show that BPC6 was required and sufficient to recruit LHP1 to GAGA motif-containing DNA probes in vitro. We also found that LHP1 interacts with VRN2 and, therefore, can function as a possible scaffold between BPC6 and VRN2. The lhp1-4 bpc4 bpc6 triple mutant displayed a pleiotropic phenotype, extreme dwarfism and early flowering, which disclosed synergistic functions of LHP1 and group II plant BPC members. Transcriptome analyses supported this synergy and suggested a possible function in the concerted repression of homeotic genes, probably through histone H3 lysine-27 trimethylation. Hence, our findings suggest striking similarities between animal and plant GAGA-binding factors in the recruitment of PRC1 and PRC2 components to Polycomb-responsive DNA element-like GAGA motifs, which must have evolved through convergent evolution.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / metabolism*
  • Carrier Proteins / metabolism
  • Chromosomal Proteins, Non-Histone / chemistry
  • Chromosomal Proteins, Non-Histone / metabolism*
  • DNA-Binding Proteins / metabolism*
  • Gene Expression Regulation, Plant
  • Genetic Loci
  • Genetic Pleiotropy
  • Histones / metabolism
  • Lysine / metabolism
  • Methylation
  • Models, Biological
  • Mutation / genetics
  • Nuclear Proteins / metabolism
  • Nucleotide Motifs / genetics*
  • Polycomb-Group Proteins / metabolism*
  • Protein Binding
  • Protein Multimerization
  • Protein Structure, Tertiary

Substances

  • Arabidopsis Proteins
  • BPC6 protein, Arabidopsis
  • Carrier Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Histones
  • Nuclear Proteins
  • Polycomb-Group Proteins
  • TFL2 protein, Arabidopsis
  • VRN2 protein, Arabidopsis
  • Lysine