Heterochromatin re-organization associated with the transcriptional reprogramming under viral infection inArabidopsis

Abstract

Epigenetic mechanisms are key regulators of genomic integrity and genic expression. Emerging evidence shows that epigenetic regulation 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 are 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. Altogether, our results provide a complete picture of the epigenetic changes that occur during biotic stress and exemplify the overall dynamism of epigenetic regulation in eukaryotic organisms.

Hop stunt viroid infection alters host heterochromatin

“…In line with this accumulation pattern and the canonical role of both repressive marks, repeats are transcriptionally reactivated at later infection points, while genes are mostly affected by gain of H3K27me3. Similar results were recently obtained in virus-infected plants, where a catalytic component of the PRC2 complex (CURLY LEAF) was identified as a factor promoting viral tolerance (37), and in general H3K27me3 homeostasis is an important mark regulating both the stress response (38,92) and developmental cues (22–28).…”

“…H3K9me2 and H3K27me3 are the main histone marks delimiting plant heterochromatin (79). In Arabidopsis, H3K27me3 can “invade” constitutive heterochromatic regions under heavy loss of DNA methylation and/or heterochromatic identity in mutants, or under viral stress (37,80,81). Interestingly, despite the overall reprogramming of the two marks observed during viroid infection (Fig 2 and Fig 3), there was a minimal interaction (if any) between the loss and gain of any of the repressive histone marks (Fig 4C and Fig 4E).…”

“…Previous analysis of the interaction between the repressive histone marks H3K9me2 and H3K27me3 have identified a compensatory mechanism where H3K27me3 invades H3K9me2 regions in mutant backgrounds that lose constitutive heterochromatin (80,81) or under CMV infection (37). Here we were not able to identify a similar mechanism, an indeed, despite the strong symptomatology displayed by plants infected with HSVd (similar to CMV) the two heterochromatic marks retained their identity.…”

“…Particularly, DNA methylation is a dynamic stress-responsive epigenetic mark under both biotic and abiotic stresses (39–51) that can even be transmitted transgenerationally (52,53). Additionally, histone marks have been proposed to play a role in regulation of the stress-associated transcriptional reprogramming (35,54–60) although their dynamism and role under stress in plants has not been studied in detail until recently (37,38,61).…”