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Disease Is Optional: The Surprising Abundance of Facultative Fungal Plant Pathogens
Elizabeth J Indermaur1, Nathaniel M Westrick1
1Connecticut Agricultural Experiment Station, Valley Laboratory, Windsor, CT, U.S.A.
Abstract:
Plant pathology has a long history of categorizing fungal pathogens according to discrete nutritional lifestyles. Although 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 that 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, in which 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 toward 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.
Insights
Many plant-pathogenic fungi are facultative pathogens, colonizing plants without causing disease until specific conditions arise. This challenges traditional classifications and highlights the ecological flexibility of fungi.
Area of Science:
- Plant Pathology
- Mycology
- Ecology
Background:
- Traditional classification of fungal pathogens relies on discrete nutritional lifestyles.
- This categorization implies disease is a defining microbial trait, challenged by ecological and genomic evidence.
- Overreliance on model organisms may bias understanding of fungal ecological flexibility.
Purpose of the Study:
- To propose 'facultative pathogenicity' as a dominant state for many plant-associated fungi.
- To challenge existing conceptual frameworks in plant pathology.
- To encourage research into the ecological and physiological conditions governing plant-fungal interactions.
Main Methods:
- Phylogenetic analysis
- Genomic data synthesis
- Ecological data review
- Cross-taxa evidence synthesis
Main Results:
- Many plant-associated fungi shift dynamically between endophytism and necrotrophy.
- Widespread asymptomatic colonization of hosts by diverse fungal taxa was demonstrated.
- Environmental, developmental, genetic, and biochemical cues catalyze transitions to disease.
Conclusions:
- Facultative pathogenicity, not obligate disease, is likely the dominant state for many fungi.
- Reframing fungi as facultative pathogens impacts classification, resistance studies, and experimental design.
- Recognizing disease as one outcome necessitates studying conditions governing plant-fungal associations.
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