Epigenetic control of effector gene expression in the plant pathogen fungus Leptosphaeria maculans

Abstract<br/>Abstract

英语. Plant pathogens secrete an arsenal of small secreted proteins (SSPs) acting as effectors that modulate host immunity to facilitate infection. In Eukaryotic phytopathogens, SSP-encoding genes are often located in particular genomic environments and show waves of concerted expression during plant infection. To date, little is known about the regulation of their expression. Leptosphaeria maculans is an ascomycete fungus responsible for stem canker of oilseed rape. Its genome has a bipartite structure alternating gene rich GC-equilibrated isochores and gene poor AT-isochores made up of mosaics of transposable elements. The AT-isochores encompass one third of the genome and are enriched in putative effector genes that present the same expression pattern (no or a low expression level during in vitro growth and a strong over-expression during primary infection). Here, we investigated the involvement of one histone modification, histone H3 lysine 9 methylation (H3K9me3), in epigenetic regulation of concerted effector gene expression in L. maculans. For this purpose, we silenced expression of two key players in heterochromatin assembly and maintenance, HP1 and DIM5, by RNAi. By using HP1-GFP as a heterochromatin marker, we observed that almost no chromatin condensation is visible in a silenced-dim5 background. Whole genome oligoarrays performed on silenced-hp1 and silenced-dim5 transformants background revealed an over-expression of pathogenicity-related genes during in vitro growth, with a favored influence on SSP-encoding genes in AT-isochores. That increase of expression during in vitro growth was associated with a reduction of H3K9 trimethylation at two SSP-encoding gene loci. These data strongly suggest that an epigenetic control, mediated by HP1 and DIM5, represses the expression of at least part of the effector genes located in AT-isochores during growth in axenic culture. Our hypothesis is that changes of lifestyle and a switch toward pathogenesis lift chromatin-mediated repression, allowing a rapid response to new environmental conditions.