Is the Pathogenic Ergot Fungus a Conditional Defensive Mutualist for Its Host Grass?

Abstract

It is well recognized, that outcomes of mutualistic plant-microorganism interactions are often context dependent and can range from mutualistic to antagonistic depending on conditions. Instead, seemingly pathogenic associations are generally considered only harmful to plants. The ergot fungus (Claviceps purpurea) is a common seed pathogen of grasses and cereals. Ergot sclerotia contain alkaloids which can cause severe toxicity in mammals when ingested, and thus the fungal infection might provide protection for the host plant against mammalian herbivores. Theoretically, the net effect of ergot infection would positively affect host seed set if the cost is not too high and the defensive effect is strong enough. According to our empirical data, this situation is plausible. First, we found no statistically significant seed loss in wild red fescue (Festuca rubra) inflorescences due to ergot infection, but the seed succession decreased along increasing number of sclerotia. Second, in a food choice experiment, sheep showed avoidance against forage containing ergot. Third, the frequency of ergot-infected inflorescences was higher in sheep pastures than surrounding ungrazed areas, indicating a protective effect against mammalian grazing. We conclude that, although ergot can primarily be categorized as a plant pathogen, ergot infection may sometimes represent indirect beneficial effects for the host plant. Ergot may thus serve as a conditional defensive mutualist for its host grass, and the pathogenic interaction may range from antagonistic to mutualistic depending on the situation.

Cross-talk of the biotrophic pathogen Claviceps purpurea and its host Secale cereale

“…Hence, the symptomless in planta growth of the fungus is not due to non-recognition because of “pollen-tube mimicry” but must have other reasons. One putative explanation might be a partially mutualistic mode of the C. purpurea -rye interaction which has been discussed earlier [39, 40]. C. purpurea causes only limited damage to the host, as only single ovaries of rye plants are infected and unlike Fusarium head blight, ergot infection does not spread from spikelet to spikelet [41, 42].…”

“…To clarify this, the suitability of alternative model host plants should be explored and included in future experimental designs. Beside the broad host range, the system is further complicated by the fact that C. purpurea infection might also provide benefit for the host plant [40]. In the course of evolution this could lead to increased tolerance towards C. purpurea infection even despite the lack of individual effectors.…”

Toward Comprehensive Plant Microbiome Research

“…Meanwhile, an increasing number of evolutionary ecology studies reveal that the same microbial species commonly occupy several ecological niches. Thus, the nature of microbe-plant interactions is labile and context-dependent in ecological and evolutionary time rather than always beneficial or disadvantageous to the host (Saikkonen et al, 1998(Saikkonen et al, , 2004Wäli et al, 2013;Rybakova et al, 2016;Selosse et al, 2018). The same microbial species might be labeled a pathogen, parasite, or endophyte, and referred to by different names.…”

Red/purple leaf margin coloration: Potential ecological and physiological functions

“…Plants also use several types of defenses that utilize other organisms. Thorny plant neighbors function as nurse plants (Rebollo et al, 2002), plant coloration may undermine herbivorous insect camouflage and increase their visibility to predators , attacked plants may emit volatile signals to alert predators of herbivore presence (Kessler and Baldwin, 2001) or use volatiles from trapped insects (LevYadun, 2014), mutualistic ants attack herbivores that approach their host plants (Huxley and Cutler, 1991), and fungal endo-or exosymbionts may provide chemical defense to their hosts (Clay, 1990;Lev-Yadun and Halpern, 2007;Wäli et al, 2013). Fig.…”