Deciphering the modes of action of Golubevia sp., an antagonist against the causal agent of powdery mildew in wheat, using an mRNA-based systems approach

Biocontrol agents are living organisms with the potential to suppress populations of plant pathogens or pests in a cropping system. The complex interplay between the different players and the changing environment, results in a combination of different modes of action. Here, we applied an mRNA-based systems approach to gain insight into the antagonist-pathogen-host interaction of Golubevia sp. isolates BC0812 and BC0850 with the causal agent of wheat powdery mildew, Blumeria graminis f. sp. tritici, in planta over time. Bioassays were performed on potted wheat plants (water-treated control, antagonist, pathogen, antagonist+pathogen) under controlled conditions. A significantly higher percentage of mildew conidia were parasitized after treatment with Golubevia sp. BC0812 with 26% and BC0850 with 16% compared to the water control with 1%. Differential gene expression analysis of antagonists, pathogen and host 5, 6, 7, and 11 days after inoculation (dai) with the antagonist pointed to a combination of different modes of action: An interplay of modulating plant defense responses, impairing conidiogenesis of the pathogen by scavenging H2O2, facultative hyperparasitism and nitrogen competition. Microscopic observations supported the suggested hyperparasitism as thin mycelium could be observed on Bgt conidia at 6 dai and later. Taken together the results allowed the formulation of new hypothesis regarding modes of action and the interplay between antagonist, pathogen and host. It showed that a solid molecular understanding of the antagonist-pathogen relationship over time is essential for less biased mode of action studies. Understanding this complex interplay is the basis for targeted optimization strategies and allows discovery of new potential targets and markers for future biocontrol development.

Automated summary

Biocontrol agents like Golubevia sp. BC0812 and BC0850 show significant parasitic effects on the wheat powdery mildew pathogen, impairing its conidiogenesis. Gene expression analysis revealed a combination of different modes of action including modulating plant defense responses, scavenging H2O2 to impair pathogen conidiogenesis, potential hyperparasitism, and nitrogen competition. These findings highlight the importance of understanding the complex interplay between antagonist, pathogen, and host for targeted optimization strategies in biocontrol development.