Obligate biotroph pathogens defend their niche against competing microbes by keeping host defense at a functional level

Recent research has given insights into how plants behave under single and combined abiotic and biotic stress conditions in a controlled environment, highlighting the challenges and need for experiments under natural conditions where plants have to adapt to a variety of environmental stresses during their growth period. In nature, a broad diversity of microbes colonizes the phyllosphere and rhizosphere causing biotic stress. One of the most common diseases on wild Brassicaceae, like Arabidopsis thaliana, is the obligate biotroph oomycete genus Albugo, causal agent of white rust. Biotrophic, as well as hemibiotrophic plant pathogens interact efficiently with the host plant and suppress host defense responses. Lab experiments have even shown that Albugo sp. are able to suppress non-host resistance and therefore enable pathogens to grow that are otherwise avirulent. We asked how a pathogen that is vitally dependent on a living host can compete in nature for limited niche space while paradoxically enabling colonization of its host plant for competitors. To address this question, we used a proteomics approach to identify differences and commonalities between lab and field samples of Albugo sp.-infected and -uninfected Arabidopsis thaliana plants. We could identify highly similar protein profiles in infected and uninfected plants. In wild plants, however, a broad range of defense related proteins were detected in the apoplast regardless of infection status, while no, or low levels of defense-related proteins were detected in lab samples. These results indicate that Albugo sp. do not trigger strong immune responses and leave distinct branches of the immune signaling network intact. To validate our findings, and to get mechanistic insights, immune-induced and -compromised A. thaliana plants were tested with different biotrophic pathogens. Our findings reveal how the biotroph pathogen Albugo selectively interferes with host defense under different environmental conditions and competitive pressure to maintain its ecological niche. Adaptation to host immune responses and maintaining a partially active host immunity seems advantageous against competitors. We suggest a model for future research that considers not only host-microbe but in addition microbe-microbe and microbe-host-environment factors.