Re-Envisioning the Plant Disease Triangle: Full Integration of the Host Microbiota and a Focal Pivot to Health Outcomes.

Abstract

The disease triangle is a structurally simple but conceptually rich model that is used in plant pathology and other fields of study to explain infectious disease as an outcome of the three-way relationship between a host, a pathogen, and their environment. It also serves as a guide for finding solutions to treat, predict, and prevent such diseases. With the omics-driven, evidence-based realization that the abundance and activity of a pathogen are impacted by proximity to and interaction with a diverse multitude of other microorganisms colonizing the same host, the disease triangle evolved into a tetrahedron shape, which features an added fourth dimension representing the host-associated microbiota. Another variant of the disease triangle emerged from the recently formulated pathobiome paradigm, which deviates from the classical "one pathogen" etiology of infectious disease in favor of a scenario in which disease represents a conditional outcome of complex interactions between and among a host, its microbiota (including microbes with pathogenic potential), and the environment. The result is a version of the original disease triangle where "pathogen" is substituted with "microbiota." Here, as part of a careful and concise review of the origin, history, and usage of the disease triangle, I propose a next step in its evolution, which is to replace the word "disease" in the center of the host-microbiota-environment triad with the word "health." This triangle highlights health as a desirable outcome (rather than disease as an unwanted state) and as an emergent property of host-microbiota-environment interactions. Applied to the discipline of plant pathology, the health triangle offers an expanded range of targets and approaches for the diagnosis, prediction, restoration, and maintenance of plant health outcomes. Its applications are not restricted to infectious diseases only, and its underlying framework is more inclusive of all microbial contributions to plant well-being, including those by mycorrhizal fungi and nitrogen-fixing bacteria, for which there never was a proper place in the plant disease triangle. The plant health triangle also may have an edge as an education and communication tool to convey and stress the importance of healthy plants and their associated microbiota to a broader public and stakeholdership.