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

ABSTRACT: 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.

ORGANISM(S): Auriculariopsis ampla

PROVIDER: GSE132826 | GEO | 2019/06/18

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

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