Metabolic convergence on TOR signaling in the chestnut blight fungus and its regulation by host plant signals

Summary Transcriptomic analysis of the chestnut blight fungus Cryphonectria parasitica identified 22 core genes regulated by Cryphonectria hypovirus 1 (CHV1) infection and sectorization. Twelve genes with common phenocopies were analyzed: all mutants displayed restricted colonial growth, intense pigmentation, hyperbranched terminal hyphae with swollen globose cells, and reduced conidiation. Although gene‐specific mutant phenotypes existed, responses to most stressors were similar to those of the wild‐type. Mutant growth was highly sensitive to nutrient conditions, and growth restriction was notably alleviated by supplementation with 1.0 M sorbitol, nutrient‐deficient media, or skim milk. All mutants showed hallmarks consistent with reduced target of rapamycin (TOR) signaling. Trehalose accumulation, a canonical fungal response to TOR inhibition, was observed in mutants via transcriptional upregulation of core trehalose biosynthetic genes, resulting in altered hyphal osmolarity and common mutant cell phenotypes. Plant signals overrode the mutants' phenotypes, strongly promoting their growth and differentiation. Although a severely retarded growth defect was observed in mutants, mutants' virulence remained intact, which can be ascribed to the host‐plant signals. Cryphonectria hypovirus 1 (CHV1)‐infected mutants exhibited greater growth restriction, accompanied by genotype‐specific CHV1 titers. Despite gene‐specific variation, common phenocopies indicate that diverse metabolic pathways converge on the TOR pathway in the fungal response to host‐plant and CHV1 infection.