DNA METHYLTRANSFERASE 1 is involved in (m)CG and (m)CCG DNA methylation and is essential for sporophyte development in Physcomitrella patens

Plant Mol Biol. 2015 Jul;88(4-5):387-400. doi: 10.1007/s11103-015-0328-8. Epub 2015 May 6.

Abstract

DNA methylation has a crucial role in plant development regulating gene expression and silencing of transposable elements. Maintenance DNA methylation in plants occurs at symmetrical (m)CG and (m)CHG contexts ((m) = methylated) and is maintained by DNA METHYLTRANSFERASE 1 (MET1) and CHROMOMETHYLASE (CMT) DNA methyltransferase protein families, respectively. While angiosperm genomes encode for several members of MET1 and CMT families, the moss Physcomitrella patens, serving as a model for early divergent land plants, carries a single member of each family. To determine the function of P. patens PpMET we generated ΔPpmet deletion mutant which lost (m)CG and unexpectedly (m)CCG methylation at loci tested. In order to evaluate the extent of (m)CCG methylation by MET1, we reexamined the Arabidopsis thaliana Atmet1 mutant methylome and found a similar pattern of methylation loss, suggesting that maintenance of DNA methylation by MET1 is conserved through land plant evolution. While ΔPpmet displayed no phenotypic alterations during its gametophytic phase, it failed to develop sporophytes, indicating that PpMET plays a role in gametogenesis or early sporophyte development. Expression array analysis revealed that the deletion of PpMET resulted in upregulation of two genes and multiple repetitive sequences. In parallel, expression analysis of the previously reported ΔPpcmt mutant showed that lack of PpCMT triggers overexpression of genes. This overexpression combined with loss of (m)CHG and its pleiotropic phenotype, implies that PpCMT has an essential evolutionary conserved role in the epigenetic control of gene expression. Collectively, our results suggest functional conservation of MET1 and CMT families during land plant evolution. A model describing the relationship between MET1 and CMT in CCG methylation is presented.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcohol Oxidoreductases
  • Base Sequence
  • Bryopsida / genetics*
  • Bryopsida / growth & development
  • Bryopsida / metabolism*
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism*
  • DNA Methylation* / genetics
  • DNA, Plant / genetics
  • DNA, Plant / metabolism
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Models, Biological
  • Molecular Sequence Data
  • Mutation
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plants, Genetically Modified

Substances

  • DNA, Plant
  • Plant Proteins
  • Alcohol Oxidoreductases
  • lactate-malate transhydrogenase
  • DNA (Cytosine-5-)-Methyltransferases
  • chromomethylase