Disease Is Optional: The Surprising Abundance of Facultative Fungal Plant Pathogens

Plant pathology has a long history of categorizing fungal pathogens according to discrete nutritional lifestyles. While this is expedient for practical management efforts, this categorization often implies that disease is a defining property of the microbe, despite increasing ecological, genomic, and experimental evidence which challenges this implication. To describe the many plant-associated fungi that break this mold, we suggest adopting an encompassing term. Here, we hypothesize that facultative pathogenicity, where fungi colonize plants asymptomatically and induce disease only under specific conditions, is not an exception but the dominant state of many plant-pathogenic fungi. We further suggest that an overreliance on obligate biotrophs and other model organisms has biased conceptual frameworks and prevented our recognition of the ecological flexibility of many fungal plant pathogens. Drawing on phylogenetic, genomic, and ecological data, we show that many plant-associated fungi shift dynamically along a continuum from endophytism to necrotrophy. This evidence is synthesized across diverse fungal taxa demonstrating widespread asymptomatic colonization of hosts and highlights how environmental, developmental, genetic, and biochemical cues catalyze transitions to disease. Reframing our thinking about many of these fungi as facultative pathogens challenges prevailing concepts of pathogenic lifestyle classification, nonhost resistance, and experimental design in plant pathology. Recognizing disease as one possible outcome, rather than a defining trait, of plant-fungal interactions invites a conceptual shift towards studying the ecological and physiological conditions that govern these associations, with diverse implications for the study of these fungi and the management of their resulting diseases.