(Decoy) Amplicon-sequencing (UNPUBLISHED)
Plant roots host complex microbial communities that are essential for nutrient uptake, growth, and resistance to disease. Fungal pathogens can disrupt root microbiota, leading to dysbiosis and reduced yields. While plants defend themselves through innate immunity and microbial antifungal activity, a less-explored strategy to limit pathogen colonization is manipulating environmental carbon. Pathogenic fungi rely on carbohydrate-active enzymes whose expression is strongly influenced by carbon availability. Yet, how carbon sensing regulate fungal pathogenicity remains largely unexplored. Here, we show that inoculation of specialized methylated-sugar can act as metabolic decoys, significantly protecting plants from fungal pathogens. High-throughput carbon screening revealed that 3-O-methylglucose (3-OMG) and C2-epimers protect against fungal pathogens by accumulating in fungal cells without being metabolized, repressing pectin- and cellulose-degrading enzymes. 3-OMG also induces mild, host-specific decoy activity in Arabidopsis, dependent on developmental stage. At the microbiota level, 3-OMG is a poor carbon source for most microbes, but in multi-kingdom synthetic communities, Pseudomonas, via PQQ-dependent dehydrogenases, can cross-feed fungal strains, enabling significant 3-OMG consumption. Greenhouse assays confirmed robust 3OMG protection against all fungal pathogens tested on arabidopsis, rapeseed and grapevine, highlighting the potential of metabolic decoys to protect economically important crops. These results demonstrate that metabolic decoying of nutrient signals provides an effective strategy for controlling fungal diseases with mild enviromental impact. We hope our study will pave the way for discovering additional metabolic decoys, offering a sustainable strategy to protect crops from both biotic and abiotic stresses.
Plant roots host complex microbial communities that are essential for nutrient uptake, growth, and resistance to disease. Fungal pathogens can disrupt root microbiota, leading to dysbiosis and reduced yields. While plants defend themselves through innate immunity and microbial antifungal activity, a less-explored strategy to limit pathogen colonization is manipulating environmental carbon. Pathogenic fungi rely on carbohydrate-active enzymes whose expression is strongly influenced by carbon availability. Yet, how carbon sensing regulate fungal pathogenicity remains largely unexplored. Here, we show that inoculation of specialized methylated-sugar can act as metabolic decoys, significantly protecting plants from fungal pathogens. High-throughput carbon screening revealed that 3-O-methylglucose (3-OMG) and C2-epimers protect against fungal pathogens by accumulating in fungal cells without being metabolized, repressing pectin- and cellulose-degrading enzymes. 3-OMG also induces mild, host-specific decoy activity in Arabidopsis, dependent on developmental stage. At the microbiota level, 3-OMG is a poor carbon source for most microbes, but in multi-kingdom synthetic communities, Pseudomonas, via PQQ-dependent dehydrogenases, can cross-feed fungal strains, enabling significant 3-OMG consumption. Greenhouse assays confirmed robust 3OMG protection against all fungal pathogens tested on arabidopsis, rapeseed and grapevine, highlighting the potential of metabolic decoys to protect economically important crops. These results demonstrate that metabolic decoying of nutrient signals provides an effective strategy for controlling fungal diseases with mild enviromental impact. We hope our study will pave the way for discovering additional metabolic decoys, offering a sustainable strategy to protect crops from both biotic and abiotic stresses.