Endophytes are increasingly recognized as modifying host plant disease (e.g., pathogen antagonists that reduce plant disease severity), suggesting promise for their use in crop disease management. However, pathogen antagonism is inconsistently expressed, often for unknown reasons. We sought to elucidate the rules governing endophyte disease modification to inform microbiome manipulations in agriculture. We tested whether pathogen competition influences pathogen antagonism in three field inoculation experiments. Using the black cottonwood of the Pacific Northwest (Populus trichocarpa) as a model system, we evaluated whether competition for leaf mesophyll cells between a Melampsora rust pathogen and a microscopic, eriophyid mite affects rust pathogen antagonism by fungal leaf endophytes. We varied mite-rust competition by utilizing Populus genotypes characterized by differential genetic resistance to the two organisms.
Two contingency rules emerged from our inoculation experiments: 1) pathogen antagonism by endophytes can be preempted by host genes for resistance that suppress pathogen development in the first place, and 2) pathogen antagonism can secondarily be preempted by competitive exclusion of the rust by the mite. Our results suggest a Populus defense hierarchy with resistance genes on top, followed by pathogen competition, and finally by pathogen antagonism. We expect that geographic variation in the abundance and distribution of the mite will heavily impact the scaling of plant-endophyte mutualisms, and the suitability of endophyte applications for disease management in poplar plantations in the Pacific Northwest.