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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

In July 2020, plants with crinkled, chlorotic, occasionally necrotic leaves, typical for Soybean Mosaic Virus (SMV), were observed in eight soybean fields (Glycine max L.) in Flevoland, The Netherlands (Supp. Fig. 1). Disease incidence varied from 5-50% and the plants affected often occurred in small or extensive patches. Leaves from several symptomatic plants were sampled from each of two fields planted with soybean variety Green Shell or Summer Shell. Total RNA was extracted from one plant leaf sample per field using InviTrap Spin Plant RNA Mini Kit (Invitek, Germany). One-tube RT-PCRs employing potyvirus generic primers P9502 and CPUP (Van der Vlugt et al, 1999) and SMV-specific primers SMV-dT (5'-TTTTTTTTTTTTTTTAGGACAAC-3') and SMV-Nib-Fw (5'-CAAGGATGARTTTAAGGAG-3') combined with Sanger sequencing confirmed the presence of SMV in all leaf samples. To exclude the presence of other agents in the samples, total RNA from each cultivar was used in standard Illumina library preparation with ribosomal RNA depletion followed by sequencing on an Illumina NovaSeq6000 (paired-end, 150 bp) which yielded 66,579,158 reads (Summer Shell) and 223,953,206 reads (Green Shell). After quality trimming in CLC Genomics Workbench 20.0.4 (CLC-GWB; Qiagen, Hilden), four million reads were randomly sampled for de novo assembly. Contigs over 500 nucleotides (nts) in length with a minimum of 500 reads were annotated by BLASTn against NCBI GenBank. This identified one contig of 9,883 nts (6,233,397 reads) in Summer Shell and one contig of 9,727 nts (3,139,927 reads) in Green Shell with clear homology to SMV (E-value = 0.0). No other viruses were identified in the datasets. Reference assemblies against the SMV reference sequence (NC_002634) mapped 24,090,763 reads (36.2%) for Summer Shell and 175,459,637 reads (78.3%) for Green Shell. Extracted consensus sequences for SMV in both soybean cultivars were 9,584 nts long (excluding the poly-A tail). Sequence data from the de novo and referenc

Looking forward includes looking back every now and then. In 2007, David Weller looked back at 30 years of biocontrol of soil-borne pathogens by Pseudomonas and signified that the progress made over decades of research has provided a firm foundation to formulate current and future research questions. It has been recognized for more than a century that soil-borne microbes play a significant role in plant growth and health. The recent application of high-throughput omics technologies has enabled detailed dissection of the microbial players and molecular mechanisms involved in the complex interactions in plant-associated microbiomes. Here, we highlight old and emerging plant microbiome concepts related to plant disease control, and address perspectives that modern and emerging microbiomics technologies can bring to functionally characterize and exploit plant-associated microbiomes for the benefit of plant health in future microbiome-assisted agriculture.