title: Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans.
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.
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Jessica L
authors.initials: JL
authors.lastname: Soyer
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Mennat
authors.initials: M
authors.lastname: El Ghalid
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Glaser
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Bénédicte
authors.initials: B
authors.lastname: Ollivier
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Juliette
authors.initials: J
authors.lastname: Linglin
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Jonathan
authors.initials: J
authors.lastname: Grandaubert
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Marie-Hélène
authors.initials: MH
authors.lastname: Balesdent
authors.affiliation: Department of Biochemistry and Biophysics, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Lanelle R
authors.initials: LR
authors.lastname: Connolly
authors.affiliation: Department of Biochemistry and Biophysics, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Michael
authors.initials: M
authors.lastname: Freitag
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Thierry
authors.initials: T
authors.lastname: Rouxel
authors.affiliation: INRA, UR 1290 BIOGER-CPP, Thiverval-Grignon, France.
authors.forename: Isabelle
authors.initials: I
authors.lastname: Fudal
mesh_terms: D001203:Ascomycota / Q000235:genetics* / Q000472:pathogenicity; D029688:Brassica napus / Q000235:genetics / Q000382:microbiology; D044127:Epigenesis, Genetic / Q000235:genetics*; D015966:Gene Expression Regulation, Fungal; D006570:Heterochromatin / Q000235:genetics*; D011495:Histone-Lysine N-Methyltransferase / Q000235:genetics; D006657:Histones / Q000235:genetics; D008745:Methylation; D010935:Plant Diseases / Q000235:genetics*
chemical_list: D006570:Heterochromatin; D006657:Histones; D011495:Histone-Lysine N-Methyltransferase