American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Ecological and evolutionary stabilities of biotrophism, necrotrophism, and saprotrophism”

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Sayaki U. Suzuki and Akira Sasaki (July 2019)

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Diverse trophic strategies of fungi are studied theoretically, revealing novel insight into their control and evolution

How to eat something: Fresh while alive? Murder and munch? Or let them rot before devouring?

Examples of typical three fungi (bio-/necro-/saprotroph) based on their trophic strategies. <i>Puccinia reconditea</i> parasitizes on living wheat leaves. <i>Fusarium oxysporum</i> invades into host vascular (in center panel, a vascular browning occurs in the tomato root) and then causes wilting of the entire seedling. <i>Marasmius maximus</i> absorbs nutrients from litters in forest environment. <br />(Photo credits: left by Yasuo Ohto; center and right by Sayaki U. Suzuki)
Examples of typical three fungi (bio-/necro-/saprotroph) based on their trophic strategies. Puccinia reconditea parasitizes on living wheat leaves. Fusarium oxysporum invades into host vascular (in center panel, a vascular browning occurs in the tomato root) and then causes wilting of the entire seedling. Marasmius maximus absorbs nutrients from litters in forest environment.
(Photo credits: left by Yasuo Ohto; center and right by Sayaki U. Suzuki)

Fungi have diverse strategies for utilizing plants as their nutrient resources. For example, obligate biotrophs like wheat leaf rust reproduce in living hosts, obligate necrotrophs like take-all fungi kill infected hosts and reproduce in dead material, while obligate saprotrophs like fairy ring mushrooms reproduce only in dead plant residues in the environment. What is the most efficient trophic strategy for fungi to utilize a given plant population while ecologically sustaining it? How have such diverse trophic strategies evolved in fungi? To tackle these questions, Sayaki U. Suzuki at CARC/NARO and Akira Sasaki at SOKENDAI attempted to construct an epidemiological model that explores three trophic modes (biotrophic, necrotrophic and saprotrophic transmissions) for fungi to utilize plants. Although their model is simple, consisting only of four states of host plants (susceptible living plant, infected living plant, uninfected dead plant, and infected dead plant), it adequately describes the ecological behavior of plant pathogenic fungi.

Using this model, they obtained the threshold condition for the spread of the disease epidemic and reorganized the conventional physiological classification of fungi from the ecological perspective. They then proposed four types of ecological groups corresponding to the patterns of dependence on nutrient resources, either living or dead plants. It is also possible to draw guidelines from this model for controlling crop diseases suitable for each fungal type of nutrient dependency.

By analyzing the evolution of virulence in their plant-fungi model, they found that a milder fungal virulence in living plants is always selected for if plant-fungi populations are in a stable (endemic) state. However, with a sufficiently strong necrotrophic transmission rate, the host population densities show sustained cycles, which promotes the evolution towards higher virulence. They refer to this self-reinforcement towards highly virulent necrotrophs as “necrotrophic spiral”.


Abstract

Fungi have multiple trophic behaviors including biotrophism (parasitism on living hosts), necrotrophism (parasitism through killing host tissues), and saprotrophism (feeding on decaying organic matter). Historical classifications of plant pathogens are based on many different axes, including their trophic dependence on living and dead plants, their pathogenicity and mutualistic relationship to host plants, and their transmission pathways and infection mechanisms. Such diverse classifications are sometimes conflicting with each other. Clarifying the delineations among these groups would promote synthesis of fungal biology with current ecological and evolutionary concepts. To ask when biotrophic, necrotrophic, or saprotrophic fungi are maintained and are favored by selection, we constructed an epidemiological model that describes the transitions between four states of host plants: susceptible living plant (S), infected living plant (I), uninfected dead plant (D), and infected dead plant, or plant residue (R). S and D represent two kinds of resource—living and dead plant tissues—for fungal inocula (I and R). We obtained values for the basic reproductive number (R0), which defines the persistence criteria of fungi. Based on our results, we propose four types of ecological groups corresponding to the patterns of dependence on nutrient resources: (i) parasitism-dependent fungi, characterized by their critical dependence on living plants; (ii) saprotrophism-dependent fungi, characterized by their critical dependence on dead plants; (iii) facultatively dependent fungi, which are neither parasitism nor saprotrophism dependent; and (iv) doubly dependent fungi, which are neither wholly parasitism dependent nor wholly saprotrophism dependent. This grouping can be used to suggest principles for effective pest control. Our model also reveals simple conditions for the evolution of fungal trophic behaviors. We found that, in the absence of a trade-off between virulence and other life history parameters, milder fungal virulence in living plants is always selected for if plant–fungus population dynamics are stable. However, with sufficiently strong necrotrophic transmission, the host population densities show sustained cycles, which promotes the evolution of higher virulence. Epidemiological synthesis of diverse trophism in plant-fungi relationship in our model thus opens the way to discuss the evolution of fungal lifestyles as a function of ecological conditions.