Epigenetic regulation of nuclear processes in fungal plant pathogens

Abstract

Through the association of protein complexes to DNA, the eukaryotic nuclear genome is broadly organized into open euchromatin that is accessible for enzymes acting on DNA and condensed heterochromatin that is inaccessible. Chemical and physical alterations to chromatin may impact its organization and functionality and are therefore important regulators of nuclear processes. Studies in various fungal plant pathogens have uncovered an association between chromatin organization and expression of in planta-induced genes that are important for pathogenicity. This review discusses chromatin-based regulation mechanisms as determined in the fungal plant pathogen Verticillium dahliae and relates the importance of epigenetic transcriptional regulation and other nuclear processes more broadly in fungal plant pathogens.

Fig 1. A model of genome organization and epigenetic modifications in V. dahliae.

Chromosomal regions differentially display distinct chromatin features, associated with differences in 3D genome organization. (A) Representation of the chromatin structure on a linear V. dahliae chromosome. AGRs (green blocks) display a distinct open (uncondensed) chromatin profile, in which the nucleosomes are marked by tri-methylation of histone 3 lysine 27 (H3K27me3, green circles) [27]. H3K27me3-marked regions, consisting of AGRs, as well as particular regions of the core genome, are enriched for differentially expressed genes in vitro and in planta (DEGs, blue blocks) [35]. Centromeres (orange blocks) in V. dahliae, but not in all sister species are specifically associated with the LTR retrotransposon LTRE9 (pink blocks) [37]. The chromatin profile at centromeres consists of tightly packed nucleosomes that are marked by tri-methylation of histone 3 lysine 9 (H3K9me3, red circles) and by DNA-methylation (5mC, red stars) [36,37]. Besides LTRE9 TEs at the centromere, additional inactive TEs in the core genome are marked by H3K9me3 and 5mC, while active TEs in the AGRs are not associated with these marks. (B) Schematic 3D representation of the organization of 3 chromosomes in V. dahliae. Locally, genomic regions form TADs (indicated by dotted circles) that interact more strongly within the domain than with other domains. Intriguingly, TADs within AGRs are less well insulated and interact more freely with neighboring TADs [38]. Centromeres often form single TADs and display strong inter-centromeric interactions [37]. AGR, adaptive genomic region; TAD, topologically associating domain; TE, transposable element.

Fig 2. Hypothesis on epigenetic regulation of effector gene expression in fungal plant pathogens.

(A) Chromosomal regions containing effector genes (yellow blocks) are marked by heterochromatin-associated histone modifications (green circles) and the chromatin is condensed and inaccessible to transcription machinery (colored ellipses) when the pathogen does not require effector gene expression. (B) Upon plant recognition, chromosome regions containing effector genes lose their heterochromatin-associated histone modifications and the chromatin decondenses and becomes accessible to the transcription machinery.