What lurks beneath: unravelling the chemically-guided ecological interactionsof Armillaria fungi, a devastating group of subterranean forest pathogens

Armillaria species, also known as 'shoestring root-rot' and 'honey fungus' (Fig. 1A), are devastating fungal forest pathogens affecting over 500 woody plant species globally1. They are facultative necrotrophs that colonise and attack the cambium of living roots, necrotising the living tissue, and ultimately killing the tree before switching to a saprophytic phase to decay the dead tissue. Infection is established via rhizomorphs, root-like (or shoestring) structures (Fig. 1B-C), comprising fungal hyphae aggregated in parallel that form extensive underground networks in forest soils2. Rhizomorphs are exploratory organs, growing rapidly through the forest soil in search of nutrients and new hosts to infect, enabling clonal dispersal of Armillaria individuals between host plants to generate 'disease centres'. Consequently, individuals of Armillaria are the largest terrestrial organisms on the planet, with recorded individuals covering areas >900 hectares and weighing 600 tons, with estimated ages of 2500 years3. Despite the significant impacts of Armillaria species on global forestry, horticulture and agriculture, its ecological interactions and mechanisms of disease causation in natural environments are barely understood. Volatile and water-soluble chemical compounds play an important role in soil microbe-microbe and microbe-plant interactions and communication4,5, and therefore the role that plant host or rhizosphere chemistry plays in host finding of Armillaria in the soil is an important unanswered question. We hypothesise that (1) Armillaria hyphae and rhizomorphs do not grow randomly, but use chemotaxis to locate host roots, which increases the chance of host location and infection, and (2) rhizosphere and host chemistry influence Armillaria gene expression and infection dynamics in forest systems. This multidisciplinary project builds on our previous work on Armillaria species on oak6, and through leveraging advanced chemical ecology, forest pathology and gene expression7 (transcriptomics) approaches aims to generate a chemical ecogenomics framework to unravel the poorly-understood behaviour and ecology of the subterranean Armillaria pathosystem in response to host and plant rhizosphere chemistry, to inform future management strategies.