The effects of endophytic Fusarium verticillioides on the interactions of maize and its fungal pathogen Ustilago maydis.

Abstract

Diverse microbial organisms, including mycorrhizal fungi, endophytes and pathogens inhabit plants, interact with each other, and affect their fitness. Although theoretical studies suggest that the outcomes of multispecies interactions are often different from those of pairwise interactions, most empirical studies have focused on pairwise plant-pathogen interactions. Using endophytic isolates of Fusarium verticillioides (Sacc.) Nirenberg, the corn smut pathogen, Ustilago maydis DC (Corda) and maize, our studies suggest that endophytes could play important ecological roles for host defense and their impact needs to be appreciated when studying plant interactions with other organisms occurring in the same host. First, our results suggest that F. verticillioides likely interacts with U. maydis directly to reduce the host damage by pathogen infections, which we define here as 'aggressiveness.' Since the endophyte alone did not have detectable effects on plant growth, we inferred that F. verticillioides indirectly improves plant growth in the presence of the pathogen, U. maydis . Secondly, we found that U. maydis aggressiveness is constrained by the genetic association between traits governing aggressiveness and fitness, i.e., trade-off, and the endophyte, F. verticillioides enforces limits to U. maydis aggressiveness. Pathogen fitness decreases as the level of aggressiveness increases. Surprisingly, endophyte co-inoculation with the pathogen resulted in increased pathogen fitness, likely because the biotrophic pathogen, U. maydis depends on plant resources for its reproduction and plants in the endophyte co-inoculation treatments grow better than do plants in the pathogen only inoculation treatments. Lastly, we found strain-specific effects of the endophyte on the ecological and fitness outcomes of maize- U. maydis interactions. The endophyte strain which produced least amount of fusaric acid had least impact on U. maydis aggressiveness, suggesting that the secreted secondary compound of the endophyte may play antagonistic role against the pathogen. Together, these results suggest that F. verticillioides endophytes play important defensive roles for host plants and that the evolution of plant-pathogen interactions is responsive to the microbial environment in which they occur.