Abstract
Plant pathogens secrete an arsenal of small secreted proteins (SSPs) acting as effectors that modulate host immunity to facilitate infection. SSP-encoding genes are often located in particular genomic environments and show waves of concerted expression at diverse stages of plant infection. To date, little is known about the regulation of their expression. The genome of the Ascomycete Leptosphaeria maculans comprises alternating gene-rich GC-isochores and gene-poor AT-isochores. The AT-isochores harbor mosaics of transposable elements, encompassing one-third of the genome, and are enriched in putative effector genes that present similar expression patterns, namely no expression or low-level expression during axenic cultures compared to strong induction of expression during primary infection of oilseed rape (Brassica napus). Here, we investigated the involvement of one specific histone modification, histone H3 lysine 9 methylation (H3K9me3), in epigenetic regulation of concerted effector gene expression in L. maculans. For this purpose, we silenced the expression of two key players in heterochromatin assembly and maintenance, HP1 and DIM-5 by RNAi. By using HP1-GFP as a heterochromatin marker, we observed that almost no chromatin condensation is visible in strains in which LmDIM5 was silenced by RNAi. By whole genome oligoarrays we observed overexpression of 369 or 390 genes, respectively, in the silenced-LmHP1 and -LmDIM5 transformants during growth in axenic culture, clearly favouring expression of SSP-encoding genes within AT-isochores. The ectopic integration of four effector genes in GC-isochores led to their overexpression during growth in axenic culture. These data strongly suggest that epigenetic control, mediated by HP1 and DIM-5, 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.
Highlights
During infection, plant pathogenic microbes secrete a set of molecules collectively known as effectors, pathogenicity determinants that modulate plant innate immunity and enable parasitic infection [1]
We show that the genomic environment has impact on expression of Leptosphaeria maculans effector genes, and that an epigenetic mechanism that relies on two proteins involved in heterochromatin formation and maintenance, Heterochromatin Protein 1 (HP1) and DIM-5, modulates this expression, leading to repression during growth in axenic culture
Our study highlights the importance of heterochromatic landscapes, for genome maintenance and in rapid and efficient adaptation of organisms to changing environmental situations. (Brassica napus)
Summary
Plant pathogenic microbes secrete a set of molecules collectively known as effectors, pathogenicity determinants that modulate plant innate immunity and enable parasitic infection [1]. In many plant pathogenic microbes, effectors show common features They are small proteins, potentially secreted (as many possess signal peptide sequences), generally cysteine-rich and usually have no homology to known proteins in databases [3]. Bioinformatic analyses based on common features of effectors aim to identify the complete repertoire of candidate effector genes of several oomycetes [4,5] and filamentous fungi [6,7,8] These studies highlighted another common trait of effector genes: their concerted up-regulation upon plant infection which suggests co-operation between a subset of effectors at different time points [9,10]
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