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Regulation of effector gene expression as concerted waves in Leptosphaeria maculans: a two-players game

ABSTRACT: During infection, plant pathogenic fungi secrete a set of molecules collectively known as effectors, involved in overcoming the host immune defense system and in disease establishment. Effector genes are concertedly expressed as waves all along plant pathogenic fungi lifecycle. However, little is known about how coordinated expression of effector genes is regulated. Since many effector genes are located in repeat-rich regions, the role of chromatin remodeling in the regulation of effector expression was recently investigated. In Leptosphaeria maculans, causing stem canker of oilseed rape, we established that the repressive histone modification H3K9me3 (trimethylation of Lysine 9 of Histone H3), deposited by the histone methyltransferase KMT1, was involved in the regulation of expression of genes highly expressed during infection, including effectors. Nevertheless, inactivation of KMT1 did not induce expression of these genes at the same level as observed during infection of oilseed rape, suggesting that a second regulator, such as a transcription factor (TF), might be involved. Pf2, a TF belonging to the Zn2Cys6 fungal specific TF family, was described in several Dothideomycete species as essential for pathogenicity and effector gene expression. We identified the orthologue of Pf2 in L. maculans, LmPf2, and investigated the role of LmPf2 together with KMT1 in L. maculans, by inactivating and over-expressing LmPf2 in a wild type (WT) strain and a ∆kmt1 mutant. Functional analyses of the corresponding transformants highlighted an essential role of LmPf2 in the establishment of pathogenesis. Transcriptomic analyses during axenic growth showed that LmPf2 is involved in the control of effector gene expression. We observed an enhanced effect of the over-expression of LmPf2 on effector gene expression in a ∆kmt1 background, suggesting a synergic role between KMT1 and LmPf2.

ORGANISM(S): Plenodomus lingam

PROVIDER: GSE236510 | GEO | 2024/01/01

REPOSITORIES: GEO

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Project description:In plant-associated fungi, the role of the epigenome is increasingly recognized as an important regulator of genome structure and of the expression of genes involved in the interaction(s) with the host plant. Two closely-related phytopathogenic species, Leptosphaeria maculans ‘brassicae’ (Lmb) and L. maculans ‘lepidii’ (Lml) exhibit a large conservation of genome synteny but contrasted genome structure. Lmb has undergone massive invasion of its genome by transposable elements summing up one third of its genome and clustered in large TE-rich regions on chromosomal arms, while Lml genome has a low amount of repeats (3% of the genome). Previous information also showed that the TE-rich regions of Lmb host a few species-specific effector genes, expressed during plant infection, with main incidence on the adaptive potential of the fungus. The distinct genome organisation between Lmb and Lml thus provides us with a model of choice for the comparison of the epigenomic organization in two closely related phytopathogenic fungi, in order to investigate pathogenicity/effector gene landscape with respect to the chromatin landscape. To address this, we performed chromatin immunoprecipitation, targeting either histone modifications typical for heterochromatin or euchromatin, during axenic culture, combined with transcriptomic analysis to analyse the influence of the chromatin organisation on gene expression. Our data comfort in both species the postulate that facultative heterochromatin landscapes, associated with H3K27me3 domains, are enriched in genes with no annotation, including numerous candidate effector and species-specific genes. Notably orthologous genes located in the same H3K27me3 domains are enriched in genes encoding putative proteinaceous and metabolic effectors. These genes are mostly silenced in vegetative growth conditions and are likely to be involved in interaction with the host. Compared to other fungal species, including Lml, Lmb has the particularity to have large H3K9me3-domains within chromosomal arms, strongly associated to TEs, and hosting numerous species-specific effector-encoding genes. These two distinct heterochromatin landscapes hosting genes involved in interaction with the host now questions their involvement in regulation of pathogenicity, the dynamics of the domains during plant infection, and the selective advantage for the fungus to host effector genes in H3K9me3 or H3K27me3 domains.

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Regulation of effector gene expression as concerted waves in Leptosphaeria maculans: a two-players game

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