Disease-associated shifts in the rhizosphere microbiome: towards a soy-borne legacy

Plants are colonized by a wide range of microorganisms, primarily bacteria and fungi, which form the microbiome. This microbiome supports plant growth, aids nutrient uptake, and enhances disease resistance by strengthening the immune system. Plants can regulate their microbiome composition to fend off harmful microorganisms and adapt to environmental changes, such as disease, drought, and nutrient deficits. This regulation can create a protective "soilborne legacy" (SBL), a microbial soil environment that increases plant resilience against stressors over time. The SBL has been studied in Arabidopsis thaliana (Arabidopsis) under laboratory conditions. When infected with the pathogen Hyaloperonospora arabidopsidis (Hpa), Arabidopsis plants induced changes in the root microbiome, conditioning the soil for improved resistance in future plants against Hpa. We explored how Arabidopsis plants signal the recruitment of protective microbes, identifying coumarins—antimicrobial compounds regulated by the transcription factor MYB72 and enzyme F6'H1—as important contributors to SBL formation. Experiments revealed that coumarin-deficient mutants (myb72 and f6'h1) could not create a SBL, suggesting that these compounds are crucial for creating a disease-suppressive soil microbiome. Additionally, salicylic acid, a plant defense hormone, is essential for the plant’s ability to detect the SBL, as shown by salicylic acid-deficient mutants’ failure to respond to the Hpa-induced SBL. In addition to Arabidopsis, we investigated microbiome responses in commercial soybean plants, focusing on the impact of Soybean mosaic virus (SMV), a pathogen newly identified in the Netherlands. SMV infection correlated with changes in the soybean root microbiome, affecting specific bacteria and arbuscular mycorrhizal fungi. This group of fungi are beneficial for plant nutrient uptake and immunity, and were less prevalent in infected plant roots, marking a potential link between SMV and these fungi not previously known. When inoculated with both SMV and mycorrhiza, mycorrhizal fungi mitigated the growth reduction caused by SMV, highlighting their role as resilient partners in soybean cultivation. Further research examined the microbiome composition of soybean plants in U.S. fields affected by soil fungi, primarily Fusarium solani, a pathogen linked to chlorosis, necrosis, and early leaf loss. DNA sequencing identified Fusarium solani as a major contributor to the disease. Certain beneficial fungi were enriched in healthy plants, and previously linked to inhibiting Fusarium growth or enhancing plant resistance, suggesting these fungi may protect plants against F. solani. These findings underscore the potential for manipulating plant microbiomes to create disease-resistant crops. The diversity in recruited microbes suggests that plants attract a variety of functionally similar but taxonomically diverse organisms, depending on the pathogen, plant genotype, and soil composition. Future work should focus on identifying specific plant signaling molecules involved in microbiome recruitment and assess their relevance across different crops and field conditions. This research may guide the development of microbial products as eco-friendly agricultural tools, enhancing crop resilience without reliance on chemical treatments.