Parallels in fungal pathogenesis on plant and animal hosts

Fungi are important pathogens of plants and cause more significant yield losses than bacteria or viruses. However, bacteria and viruses are more important than fungi as pathogens of animals; indeed, whether or not a fungus even becomes pathogenic on an animal often depends on the immune status of the host. Until the rapid rise of opportunistic fungal infections in humans, pathogenicity mechanisms in plant pathogens were better understood than those in animal pathogens. Increased research activity in medical mycology has coincided with the development of molecular genetic and genomic resources, which are being exploited to develop a detailed understanding of fungal pathogenesis in both animals and plants. Several constraints and peculiarities govern the types of information that can be derived from such studies. For instance, analyses of human-pathogenic fungi generally rely on cell lines and experimental animal models, in contrast to plant pathogens, which can be studied directly on their hosts. Many more fungal species infect plants than animals, and thus, more plant-fungus systems than animal-fungus systems are studied. This is mainly because there are far more plant hosts than animal hosts that are of economic importance, with the obvious exception of human disease, and because plants can be manipulated without the ethical issues associated with animal experimentation.

Pathogenesis involves the interaction of two partners with input from the environment, a concept described as the 'disease triangle' in plant pathology. A more recent concept developed for animal pathogens is the 'damage-response' framework which emphasizes that the outcome of an interaction is determined by the amount of damage incurred by the host (16). These concepts are useful reminders of the complexity of the interaction, as opposed to focusing on just the individual partners (host and pathogen). Surprisingly, there are few reports of fungal pathogenesis that describe commonalities of mechanisms for plants and animals. A commentary published nearly 10 years ago discussed issues such as degradation of the host, pathogen differentiation, regulatory genes, and signal transduction (37). These topics are still relevant, and an abundance of new information about them is available. This review describes parallels in fungal pathogenesis in plant and animal hosts, focusing on ascomycetes, as members of this phylum are generally well characterized. In general, four classes of ascomycetes are rich in plant pathogens (Dothideomycetes, Leotiomycetes, Sordariomycetes, and Taphrinomycetes), while animal pathogens generally belong to another two classes (Chaetothyriomycetes and Eurotiomycetes) that contain few plant pathogens (10). However, several ascomycete species can infect both animal and plant hosts, thus making it easier to identify commonalities of disease mechanisms. Other fungal phyla, particularly Basidiomycota, include important, well-characterized plant and animal pathogens (e.g., Ustilago maydis and Cryptococcus neoformans). These are reviewed extensively elsewhere (28, 41). Far less is known about the diseases caused by fungi from other phyla, including zygomycete diseases of humans and chytrid diseases of amphibians, as these are uncommon and are also challenging systems for experimental work. Although we emphasize the parallels in fungal pathogenesis in plant and animal hosts, in some cases we highlight a feature that has as yet been discovered only in either animal or plant pathogens but that may apply to both and thus lead to an enhanced understanding of disease mechanisms.

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