Heterochromatin reorganization associated with the transcriptional reprogramming under viral infection in Arabidopsis

Epigenetic mechanisms are key regulators of genomic integrity and genic expression. Emerging evidence shows that epigenetic dynamism is an important component of the transcriptional reprogramming during stress. Despite this, the overall stress-induced reprogramming of the different epigenetic marks and their targets is unknown. Here, we uncovered multiple epigenetic changes taking place during viral infection in Arabidopsis thaliana and their connection with gene expression. We find that cucumber mosaic virus (CMV) infection induces an overall reorganization of the repressive epigenetic marks H3K9me2, H3K27me3, and DNA methylation, which interact between them and are dynamic during infection. Overall, these epigenetic changes are involved in the reprogramming of the transcriptional program to adapt to the biotic stress and might ensure genome stability through the transcriptional control of transposable elements (TEs). Mechanistically, we demonstrate that the catalytic component of the Polycomb Repressive Complex 2 (PRC2) CURLY LEAF (CLF) mediates the transcriptional repression of genes gaining H3K27me3 during viral infection and that mutants on that component induce resistance against CMV. Additionally, we identify an interaction between the virus-produced protein 2b and CLF, pointing to direct interference of H3K27me3 homeostasis by CMV. Altogether, our results provide a complete picture of the epigenetic changes taking place at repressive marks that occur during viral infection stress and exemplify the overall dynamism of epigenetic regulation in eukaryotic organisms.