Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

Abstract

Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.

Keywords: agricultural ecosystems; dynamic diversity; fungal pathogens; pathogen emergence; pathogen evolution; population genetics.

Figure 1.

Schematic illustration of agro-ecosystem field compositions based on monoculture (left) and multicultures (right). In the monoculture agro-ecosystem, one crop species is planted into a large field and treated several times during the growing season with the same pesticide. The same crop is planted and the same pesticide is applied in the following year. The resulting homogeneous environment (one selective environment per field shown in the figure) rapidly selects for specialized pathogen strains or populations that are highly adapted to this monoculture agro-ecosystem. In the multiculture agro-ecosystem, multiple crop species or cultivars of the same crop species (indicated by different patterns) are grown simultaneously in wide rows (to facilitate mechanization) in the same field. The total area planted with one crop species or crop cultivar is considerably smaller compared with the monoculture field. A series of pesticides with different modes of action is applied in wide rows (to facilitate mechanization) in an alternating pattern (orange, green and blue) over both time and space. In the following year, the same crop species or cultivars can be planted in the same field, but the respective positions of the rows can be altered and the pesticide treatments can be applied in a new alternating pattern. The net effect of the multiculture approach compared to monoculture is to confront the pathogen population with a dynamically diverse selective landscape (12 different selective environments per field shown in the figure) encompassing smaller spatial and temporal scales that forces trade-offs among traits, slowing or preventing the emergence of highly virulent and broadly adapted pathogen populations.