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Hallmarks of basidiomycete soft- and white-rot in wood-decay -omics data of Armillaria [AROC18]

ABSTRACT: The genus Armillaria spp. (Fungi, Basidiomycota) includes devastating pathogens of temperate forests and saprotrophs that decay wood. Pathogenic and saprotrophic Armillaria species can efficiently colonize and decay woody substrates, however, mechanisms of wood penetration and colonization are poorly known. We assayed the colonization and decay of autoclaved spruce roots using the conifer-specialists Armillaria ostoyae and A. cepistipes using transcriptomic and proteomic data. Transcript and protein levels were altered more extensively in the saprotrophic A. cepistipes than in the pathogenic A. ostoyae and in invasive mycelia of both species compared to their rhizomorphs. Diverse suites of carbohydrate-active enzyme genes (CAZymes), in particular pectinolytic ones and expansins, were upregulated in both species, whereas ligninolytic genes were mostly downregulated. Our gene expression data, together with previous comparative genomic and decay-chemistry analyses suggest that wood decay by Armillaria differs from that of typical white rot fungi and shows features resembling soft rot. We propose that Armillaria species have modified the ancestral white rot machinery so that it allows for selective ligninolysis based on environmental conditions and/or host types.

ORGANISM(S): Armillaria ostoyae

PROVIDER: GSE149701 | GEO | 2020/05/04

REPOSITORIES: GEO

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Hallmarks of basidiomycete soft- and white-rot in wood-decay -omics data of Armillaria [ARCE]

Project description:The genus Armillaria spp. (Fungi, Basidiomycota) includes devastating pathogens of temperate forests and saprotrophs that decay wood. Pathogenic and saprotrophic Armillaria species can efficiently colonize and decay woody substrates, however, mechanisms of wood penetration and colonization are poorly known. We assayed the colonization and decay of autoclaved spruce roots using the conifer-specialists Armillaria ostoyae and A. cepistipes using transcriptomic and proteomic data. Transcript and protein levels were altered more extensively in the saprotrophic A. cepistipes than in the pathogenic A. ostoyae and in invasive mycelia of both species compared to their rhizomorphs. Diverse suites of carbohydrate-active enzyme genes (CAZymes), in particular pectinolytic ones and expansins, were upregulated in both species, whereas ligninolytic genes were mostly downregulated. Our gene expression data, together with previous comparative genomic and decay-chemistry analyses suggest that wood decay by Armillaria differs from that of typical white rot fungi and shows features resembling soft rot. We propose that Armillaria species have modified the ancestral white rot machinery so that it allows for selective ligninolysis based on environmental conditions and/or host types.

2020-05-04 | GSE149725 | GEO

Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae

Project description:Agaricomycetes produce the most efficient enzyme systems to degrade wood and the most complex morphological structures in the fungal kingdom. Despite decades-long interest in their genetic bases, the evolution and functional diversity of both wood-decay and fruiting body formation are incompletely known.Here, we perform comparative genomic and transcriptomic analyses of wood-decay and fruiting body development in Auriculariopsis ampla and Schizophyllum commune (Schizophyllaceae), species with secondarily simplified morphologies and enigmatic wood-decay strategy and weak pathogenicity to woody plants. The plant cell wall degrading enzyme repertoires of Schizophyllaceae are transitional between those of white rot species and less efficient wood-degraders such as brown rot or mycorrhizal fungi. Rich repertoires of suberinase and tannase genes were found in both species, with tannases restricted to Agaricomycetes that preferentially colonize bark-covered wood, suggesting potential complementation of their weaker wood-decaying abilities and adaptations to wood colonization through the bark. Fruiting body transcriptomes of A. ampla and S. commune revealed a high rate of divergence in developmental gene expression, but also several genes with conserved developmental expression, including novel transcription factors and small-secreted proteins, some of the latter might represent fruiting body effectors. Taken together, our analyses highlighted novel aspects of wood-decay and fruiting body development in a widely distributed family of mushroom-forming fungi.

2019-06-18 | GSE132826 | GEO

Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria

Project description: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, appear to have acquired at least 1025 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 too, which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed putative virulence factors, extensive regulation of horizontally acquired and wood-decay related genes as well as novel noserved pathogenicity-induced small secreted proteins (PiSSPs). Two PiSSPs induced necrosis in live plants, suggesting they are potential virulence effectors conserved across Armillaria. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits, such as plant biomass degradation and pathogenicityin one of the most influential fungal pathogens of temperate forest ecosystems.

2023-06-23 | GSE235457 | GEO

Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria

2023-06-23 | GSE235456 | GEO

Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria

2023-06-23 | GSE235454 | GEO

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

Project description: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.

2023-06-20 | GSE233220 | GEO

Comparing gene expression timing and amplitude to delineate the unique pathways of brown and white rot wood-degrading fungi

Project description:Wood-degrading fungi play a critical role in global carbon cycling, and their varied mechanisms for deconstruction offer pathways for industrial bioconversion. In this study, we used comparative genomics to isolate upregulation patterns among fungi with brown rot (carbohydrate-selective) or white rot (lignin-degrading) nutritional modes. Specifically, we used whole-transcriptome profiling to compare early, middle, and late decay stages on wood wafers, matching differentially-expressed gene (DEG) patterns with fungal growth and enzyme activities. This approach highlighted 34 genes uniquely upregulated in early brown rot stages, with notable candidates involved in generating reactive oxygen species (ROS) as a pretreatment mechanism during brown rot. This approach further isolated 18 genes in late brown rot stages that may be adapted to handle oxidatively-reacted lignocellulose components. By summing gene expression levels in functional classes, we also identified a broad and reliable distinction in glycoside hydrolase (GH) versus lignocellulose oxidative (LOX) transcript counts that may reflect the energy investment burden of lignin-degrading machinery among white rot fungi.

2018-01-05 | GSE108189 | GEO

The molecular response of the white-rot fungus Dichomitus squalens to wood and non-woody biomass as examined by transcriptome and exoproteome analyses

Project description:The ability to obtain carbon and energy is a major requirement to exist in any environment. For several ascomycete fungi (post-)genomic analyses have shown that species that occupy a large variety of habitats possess a diverse enzymatic machinery, while species with a specific habitat have a more focused enzyme repertoire that is well-adapted to the prevailing substrate. White-rot basidiomycete fungi also live in a specific habitat, as they are found exclusively in wood. In this study we evaluated how well the white-rot fungus Dichomitus squalens has adapted to degrade its natural wood substrate. The transcriptome and exoproteome of D. squalens were analysed after cultivation on two natural substrates, aspen and spruce wood, and two non-woody substrates, wheat bran and cotton seed hulls. D. squalens produced ligninolytic enzymes mainly at the early time point of the wood cultures, indicating the need to degrade lignin to get access to wood polysaccharides. Surprisingly, the response of the fungus to the non-woody polysaccharides was nearly as good match to the substrate composition as observed for the wood polysaccharides. This indicates that D. squalens has preserved its ability to efficiently degrade plant polysaccharides not present in its natural habitat.

2017-01-05 | GSE79674 | GEO

LongSAGE during the initiation of ligninolytic enzymes production in Phanerochaete chrysosporium

Project description:White rot fungi are able to degrade woody lignin and other persistent organic compounds including artificial chemicals (e.g. chlorinated dioxin) in secondary metabolism. This ability has potential in a wide range of biotechnological applications including remediation of organopollutants and the industrial processing of paper and textiles. Ligninolytic fungi secondarily secrete extracellular oxidative enzymes thought to play an important role in these compounds decay. However, detail of metabolic pathway and initiation signals of the degradation system is unclear. To investigate genes directly and indirectly related to it, we constructed long serial analysis of gene expression (Long SAGE) library from the most studied white rot fungus, Phanerochaete chrysosporium. Keywords: transcriptome profiling

2007-12-31 | GSE6649 | GEO

Lineage-specific genetic innovations streamline the genomes of Armillaria species to pathogenesis

Project description:Armillaria species are devastating forest pathogens that are among the largest terrestrial organisms on Earth. They explore hosts and achieve immense colony sizes by rhizomorphs, root-like multicellular structures of clonal dispersal. To resolve the genetic bases of their unique biology, we sequenced and analyzed genomes of 4 Armillaria species and performed RNA-Seq on 7 invasive and reproductive developmental stages. Comparison with 22 basidiomycete fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose degrading enzymes and lineage-specific genes involved in rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome and share their morphogenetic machinery with fruiting bodies, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria has drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.

2017-09-15 | GSE100213 | GEO

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