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Genomic innovation and horizontal gene transfer shaped plant colonization and biomass degradation strategies of a globally prevalent fungal pathogen

ABSTRACT: Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. Armillaria species are some of the largest terrestrial organisms on Earth that cause tremendous losses in diverse ecosystems. Despite their global importance, how Armillaria evolved pathogenicity in a clade of dominantly non-pathogenic wood-degraders (Agaricales) remains elusive. Here, using new genomic data, we show that Armillaria species, in addition to widespread gene duplications and de novo gene origins, acquired at least 1,025 genes via 124 horizontal gene transfer (HGT) events, primarily from Ascomycota donors. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. HGT provides an explanation for their soft-rot like biomass degrading strategy, which is which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed extensive regulation of horizontally acquired and wood-decay related genes, putative virulence factors as well as novel conserved pathogenicity-induced small secreted proteins (PiSSPs), two of which were experimentally verified to induce necrosis in live plants. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits, such as plant biomass degradation and pathogenicity in one of the most influential fungal pathogens of temperate forest ecosystems.

ORGANISM(S): Eucalyptus grandis Armillaria luteobubalina

PROVIDER: GSE233220 | GEO | 2023/06/20

REPOSITORIES: GEO

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Project description:Wood-degrading brown rot fungi are essential recyclers of plant biomass in forest ecosystems. Their efficient cellulolytic systems, which have potential biotechnological applications, apparently depend on a combination of two mechanisms: lignocellulose oxidation by reactive oxygen species (ROS) and polysaccharide hydrolysis by a limited set of glycoside hydrolases (GHs). Given that ROS are strongly oxidizing and non-selective, these two steps are likely segregated. A common hypothesis has been that brown rot fungi use a concentration gradient of chelated metal ions to confine ROS generation inside wood cell walls before enzymes can infiltrate. We examined an alternative: that lignocellulose-oxidation (LOX) components involved in ROS production are differentially expressed by brown rot fungi ahead of GH components. We used spatial mapping to resolve a temporal sequence in Postia placenta, sectioning thin wood wafers colonized directionally. Among sections, we measured gene expression by whole transcriptome sequencing (RNAseq) and assayed relevant enzyme activities. We found a marked pattern of LOX upregulation in a narrow (5-mm; 48-hr) zone at the hyphal front, which included many genes likely involved in ROS generation. Upregulation of GH5 endoglucanases and many other GHs clearly occurred later, behind the hyphal front, with notable exceptions of two likely expansins and a GH28 pectinase. Our results support a staggered mechanism for brown rot that is controlled by differential expression rather than microenvironmental gradients. This mechanism likely results in an oxidative pretreatment of lignocellulose, possibly facilitated by expansin- and pectinase-assisted cell wall swelling, before cellulases and hemicellulases are deployed for polysaccharide depolymerization. We sequenced mRNA from 9 Postia placenta samples taken from 3 wood sections of wafer design, with 3 bioreplicates for each wood section, to compare the gene expression during brown rot processes. Three wood sections of the wafer are representing early to late decay stages.

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Genomic innovation and horizontal gene transfer shaped plant colonization and biomass degradation strategies of a globally prevalent fungal pathogen

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