Epigenetics refers to ‘the structural adaptation of chromosomal regions so as to register, receive or perpetuate altered genetic states’ (Bird [2007] Nature 447:396-398). Silencing of genes through epigenetic modifications, such as DNA cytosine methylation, is essential for plant and animal development, and for protecting genomes from invasive sequences such as tranposable elements and viruses. The 3D arrangement of chromosomes in the nucleus of resting cells is also thought to contribute to epigenetic regulation of gene expression but the mechanisms involved remain unclear. Recent work has uncovered important roles for small RNAs produced through the RNA interference (RNAi) pathway in targeting DNA methylation to specific regions of the genome (so-called RNA-directed DNA methylation [RdDM]) and in establishing blocks of silent chromatin that specify chromosome features such as centromeres. Our research combines genetic, genomic and cytological approaches in the model plant Arabidopsis thaliana to analyse problems relating to RNAi-mediated regulation of gene expression and 3D chromosome arrangement in nuclei of living plants.

RdDM has been highly elaborated in the plant kingdom and is increasingly viewed as a versatile process that contributes to plant development and stress adaptation. Forward genetic screens in our lab and others are uncovering a complex and plant-specific machinery required for RdDM, including a novel RNA polymerase Pol IV and a specialised subfamily of SNF2-like chromatin remodelling proteins. Our most recent forward screen, which is still in progress, has exploited an enhancer that is active in meristems (the plant equivalent of stem cells in mammals) to identify proteins of the RdDM machinery that are important for plant development (Figure 1).