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Plants have coevolved together with the microbes that surround them and this assemblage of host and microbes functions as a discrete ecological unit called a holobiont. This review outlines plant-driven assembly of disease-suppressive microbiomes. Plants are colonized by microbes from seed, soil, and air but selectively shape the microbiome with root exudates, creating microenvironment hot spots where microbes thrive. Using plant immunity for gatekeeping and surveillance, host-plant genetic properties govern microbiome assembly and can confer adaptive advantages to the holobiont. These advantages manifest in disease-suppressive soils, where buildup of specific microbes inhibits the causal agent of disease, that typically develop after an initial disease outbreak. Based on disease-suppressive soils such as take-all decline, we developed a conceptual model of how plants in response to pathogen attack cry for help and recruit plant-protective microbes that confer increased resistance. Thereby, plants create a soilborne legacy that protects subsequent generations and forms disease-suppressive soils.

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 pr