Ectopic Application of the Repressive Histone Modification H3K9me2 Establishes Post-Zygotic Reproductive Isolation in Arabidopsis thaliana

Genes Dev. 2017 Jun 15;31(12):1272-1287. doi: 10.1101/gad.299347.117. Epub 2017 Jul 25.

Abstract

Hybrid seed lethality as a consequence of interspecies or interploidy hybridizations is a major mechanism of reproductive isolation in plants. This mechanism is manifested in the endosperm, a dosage-sensitive tissue supporting embryo growth. Deregulated expression of imprinted genes such as ADMETOS (ADM) underpin the interploidy hybridization barrier in Arabidopsis thaliana; however, the mechanisms of their action remained unknown. In this study, we show that ADM interacts with the AT hook domain protein AHL10 and the SET domain-containing SU(VAR)3-9 homolog SUVH9 and ectopically recruits the heterochromatic mark H3K9me2 to AT-rich transposable elements (TEs), causing deregulated expression of neighboring genes. Several hybrid incompatibility genes identified in Drosophila encode for dosage-sensitive heterochromatin-interacting proteins, which has led to the suggestion that hybrid incompatibilities evolve as a consequence of interspecies divergence of selfish DNA elements and their regulation. Our data show that imbalance of dosage-sensitive chromatin regulators underpins the barrier to interploidy hybridization in Arabidopsis, suggesting that reproductive isolation as a consequence of epigenetic regulation of TEs is a conserved feature in animals and plants.

Keywords: endosperm; heterochromatin; hybrid incompatibility; imprinted genes; polyploidy; transposable elements.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects*
  • Arabidopsis / genetics
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Plant
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase / metabolism
  • Histone-Lysine N-Methyltransferase / pharmacology*
  • Hybridization, Genetic
  • Reproductive Isolation*

Substances

  • AMETOS protein, Arabidopsis thaliana
  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase
  • SUVH9 protein, Arabidopsis