Soil structure and soil-borne diseases: using epidemiological concepts to scale from fungal spread to plant epidemics

Many epidemics of root diseases involving soil fungi depend on the interplay between fungal growth and the spatial and temporal heterogeneity of the soil environment. Colonization or infection of a root occurs at fine scales with growth and movement of fungal mycelia through soil. However, epidemics are observed at coarser scales, and depend on a cascading spread through populations of roots. We briefly review conventional analyses of soil-borne epidemics and argue that these treat soil physical conditions at scales too coarse to be meaningful for interactions between soil, plants and fungi, and fail to consider the effect of soil physical conditions on the underlying epidemiological processes. Instead, we propose a conceptual epidemiological framework that integrates spatial scales and use this to review the effect of soil structure on the dynamics of soil-borne pathogenic fungi. Using the soil-borne fungal plant pathogen Rhizoctonia solani as an example, we demonstrate that invasion of fungi into host populations is critically affected by environmental conditions operating at each of two scales: (i) at the microscopic scale (mu m - cm) the fungus preferentially explores certain pathways in soil, and small changes in soil physical conditions make the fungus switch from small, dense colonies to large, sparse and rapidly expanding ones; (ii) at the larger scale (cm - dm) a critical density of susceptible hosts is required, in excess of which fungi switch from non-invasive to invasive spread. Finally, we suggest that the approach will increase the applicability of research dealing with microscopic soil-plant-microbe interactions towards the solution of large-scale epidemiological problems.