title: Host growth can cause invasive spread of crops by soilborne pathogens.
abstract: Invasive soilborne plant pathogens cause substantial damage to crops and natural populations, but our understanding of how to prevent their epidemics or reduce their damage is limited. A key and experimentally-tested concept in the epidemiology of soilborne plant diseases is that of a threshold spacing between hosts below which epidemics (invasive spread) can occur. We extend this paradigm by examining how plant-root growth may alter the conditions for occurrence of soilborne pathogen epidemics in plant populations. We hypothesise that host-root growth can 1) increase the probability of pathogen transmission between neighbouring plants and, consequently, 2) decrease the threshold spacing for epidemics to occur. We predict that, in systems initially below their threshold conditions, root growth can trigger soilborne pathogen epidemics through a switch from non-invasive to invasive behaviour, while in systems above threshold conditions root growth can enhance epidemic development. As an example pathosystem, we studied the fungus Rhizoctonia solani on sugar beet in field experiments. To address hypothesis 1, we recorded infections within inoculum-donor and host-recipient pairs of plants with differing spacing. We translated these observations into the individual-level concept of pathozone, a host-centred form of dispersal kernel. To test hypothesis 2 and our prediction, we used the pathozone to parameterise a stochastic model of pathogen spread in a host population, contrasting scenarios of spread with and without host growth. Our results support our hypotheses and prediction. We suggest that practitioners of agriculture and arboriculture account for root system expansion in order to reduce the risk of soilborne-disease epidemics. We discuss changes in crop design, including increasing plant spacing and using crop mixtures, for boosting crop resilience to invasion and damage by soilborne pathogens. We speculate that the disease-induced root growth observed in some pathosystems could be a pathogen strategy to increase its population through host manipulation.
authors.affiliation: Institute for Genetics Environment and Plant Protection, Institut National de la Recherche Agronomique, Agrocampus Ouest, University of Rennes 1, Le Rheu, France. melenleclerc@gmail.com
authors.forename: Melen
authors.initials: M
authors.lastname: Leclerc
authors.forename: Thierry
authors.initials: T
authors.lastname: Doré
authors.forename: Christopher A
authors.initials: CA
authors.lastname: Gilligan
authors.forename: Philippe
authors.initials: P
authors.lastname: Lucas
authors.forename: João A N
authors.initials: JA
authors.lastname: Filipe
mesh_terms: D003198:Computer Simulation; D018556:Crops, Agricultural / Q000382:microbiology*; D054884:Host-Pathogen Interactions / Q000502:physiology*; D008954:Models, Biological; D010935:Plant Diseases / Q000382:microbiology* / Q000517:prevention & control; D018517:Plant Roots / Q000254:growth & development / Q000382:microbiology*; D011157:Population Dynamics; D012232:Rhizoctonia / Q000472:pathogenicity / Q000502:physiology*; D012988:Soil Microbiology