RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation

Science. 2012 Jan 6;335(6064):96-100. doi: 10.1126/science.1211651. Epub 2011 Dec 1.

Abstract

Facultative heterochromatin that changes during cellular differentiation coordinates regulated gene expression, but its assembly is poorly understood. Here, we describe facultative heterochromatin islands in fission yeast and show that their formation at meiotic genes requires factors that eliminate meiotic messenger RNAs (mRNAs) during vegetative growth. Blocking production of meiotic mRNA or loss of RNA elimination factors, including Mmi1 and Red1 proteins, abolishes heterochromatin islands. RNA elimination machinery is enriched at meiotic loci and interacts with Clr4/SUV39h, a methyltransferase involved in heterochromatin assembly. Heterochromatin islands disassemble in response to nutritional signals that induce sexual differentiation. This process involves the antisilencing factor Epe1, the loss of which causes dramatic increase in heterochromatic loci. Our analyses uncover unexpected regulatory roles for mRNA-processing factors that assemble dynamic heterochromatin to modulate gene expression.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Cell Cycle Proteins / metabolism
  • Chromatin Assembly and Disassembly*
  • Chromatin Immunoprecipitation
  • Dynactin Complex
  • Gene Expression Regulation, Fungal
  • Genes, Fungal
  • Heterochromatin / metabolism*
  • Histone-Lysine N-Methyltransferase
  • Histones / metabolism
  • Meiosis / genetics*
  • Methyltransferases / metabolism
  • Microtubule Proteins / genetics
  • Microtubule Proteins / metabolism
  • Nitrogen / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • RNA Interference
  • RNA, Fungal / genetics
  • RNA, Fungal / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces / growth & development
  • Schizosaccharomyces / metabolism*
  • Schizosaccharomyces pombe Proteins / genetics
  • Schizosaccharomyces pombe Proteins / metabolism*
  • mRNA Cleavage and Polyadenylation Factors / metabolism

Substances

  • Cell Cycle Proteins
  • Dynactin Complex
  • Heterochromatin
  • Histones
  • Microtubule Proteins
  • Mmi1 protein, S pombe
  • Nuclear Proteins
  • RNA, Fungal
  • RNA, Messenger
  • Schizosaccharomyces pombe Proteins
  • Ssm4 protein, S pombe
  • epe1 protein, S pombe
  • mRNA Cleavage and Polyadenylation Factors
  • mei4 protein, S pombe
  • Methyltransferases
  • Histone-Lysine N-Methyltransferase
  • clr4 protein, S pombe
  • Nitrogen

Associated data

  • GEO/GSE33404