SignificancePlant roots nurture a large diversity of soil microbes via exudation of chemical compounds into the rhizosphere. In turn, beneficial root microbiota promote plant growth and immunity. The root-specific transcription factor MYB72 has emerged as a central regulator in this process. Here, we show that MYB72 regulates the excretion of the coumarin scopoletin, an iron-mobilizing phenolic compound with selective antimicrobial activity that shapes the root-associated microbial community. Selected soil-borne fungal pathogens appeared to be highly sensitive to the antimicrobial activity of scopoletin, while two MYB72-inducing beneficial rhizobacteria were tolerant. Our results suggest that probiotic root-associated microbes that activate the iron-deficiency response during colonization stimulate MYB72-dependent excretion of scopoletin, thereby potentially improving their niche establishment and enhancing plant growth and protection.

Disease suppressive soils typically develop after a disease outbreak due to the subsequent assembly of protective microbiota in the rhizosphere. The role of the plant immune system in the assemblage of a protective rhizosphere microbiome is largely unknown. In this study, we demonstrate that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis. The promoted bacteria were isolated and found to interact synergistically in biofilm formation in vitro. Although separately these bacteria did not affect the plant significantly, together they induced systemic resistance against downy mildew and promoted growth of the plant. Moreover, we show that the soil-mediated legacy of a primary population of downy mildew infected plants confers enhanced protection against this pathogen in a second population of plants growing in the same soil. Together our results indicate that plants can adjust their root microbiome upon pathogen infection and specifically recruit a group of disease resistance-inducing and growth-promoting beneficial microbes, therewith potentially maximizing the chance of survival of their offspring that will grow in the same soil.

Highlights d 42% of the tested root microbiota are able to quench local root immune responses d Beneficial Pseudomonas can suppress root immunity by lowering environmental pH d Suppression of immunity facilitates root colonization by these beneficial microbes

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe-associated molecular patterns (MAMPs).However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root-invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free-living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root-invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth-defense tradeoffs triggered by the MAMP-rich rhizosphere environment. KEYWORDS host immune evasion, plant immunity, plant microbiome, rhizosphere, soil microbiology

Summary Approximately 29% of all vascular plant species are unable to establish an arbuscular mycorrhizal (AM) symbiosis. Despite this, AM fungi (Rhizophagus spp.) are enriched in the root microbiome of the nonhost Arabidopsis thaliana, and Arabidopsis roots become colonized when AM networks nurtured by host plants are available. Here, we investigated the nonhost–AM fungus interaction by analyzing transcriptional changes in Rhizophagus, Arabidopsis and the host plant Medicago truncatula while growing in the same mycorrhizal network. In early interaction stages, Rhizophagus activated the Arabidopsis strigolactone biosynthesis genes CCD7 and CCD8, suggesting that detection of AM fungi is not completely impaired. However, in colonized Arabidopsis roots, fungal nutrient transporter genes GintPT, GintAMT2, GintMST2 and GintMST4, essential for AM symbiosis, were not activated. RNA‐seq transcriptome analysis pointed to activation of costly defenses in colonized Arabidopsis roots. Moreover, Rhizophagus colonization caused a 50% reduction in shoot biomass, but also led to enhanced systemic immunity against Botrytis cinerea. This suggests that early signaling between AM fungi and Arabidopsis is not completely impaired and that incompatibility appears at later interaction stages. Moreover, Rhizophagus‐mediated defenses coincide with reduced Arabidopsis growth, but also with systemic disease resistance, highlighting the multifunctional role of AM fungi in host and nonhost interactions.

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 plantassociated 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.

Background Since the 1980s, numerous mutualistic Pseudomonas spp. strains have been used in studies on the biology of plant growth-promoting rhizobacteria (PGPR) and their interactions with host plants. In 1988, a strain from the Pseudomonas fluorescens group, WCS417, was isolated from lesions of wheat roots growing in a take-all disease-suppressive soil. In subsequent trials, WCS417 limited the build-up of take-all disease in field-grown wheat and significantly increased wheat yield. In 1991, WCS417 was featured in one of the first landmark studies on rhizobacteria-induced systemic resistance (ISR), in which it was shown to confer systemic immunity in carnation (Dianthus caryophyllus) against Fusarium wilt. The discovery that WCS417 conferred systemic immunity in the model plant species Arabidopsis thaliana in 1996 incited intensive research on the molecular mechanisms by which PGPR promote plant growth and induce broad-spectrum disease resistance in plants. Since then, the strain name appeared in over 750 studies on beneficial plant-microbe interactions. Scope In this review, we will highlight key discoveries in plant-microbe interactions research that have emerged from over 30 years of research featuring WCS417 as a model rhizobacterial strain. WCS417 was instrumental in improving our understanding of the microbial determinants that are involved in root colonization and the establishment of mutually beneficial interactions with the host plant. The model strain also provided novel insight into the molecular mechanisms of plant growth promotion and the onset and expression of rhizobacteria-ISR. More recently, WCS417 has been featured in studies on host immune evasion during root colonization, and chemical communication in the rhizosphere during root microbiome assembly. Conclusions Numerous studies on the modes of action of WCS417 have provided major conceptual advances in our understanding of how free-living mutualists colonize the rhizosphere, modulate plant immunity, and promote plant growth. The concepts may prove useful in our understanding of the molecular mechanisms involved in other binary plant-beneficial microbe interactions, and in more complex microbial community contexts, such as the root microbiome.

Pseudomonas simiae WCS417 is a root-colonizing bacterium with well-established plant-beneficial effects. Upon colonization of Arabidopsis roots, WCS417 evades local root immune responses while triggering an induced systemic resistance (ISR) in the leaves. The early onset of ISR in roots shows similarities with the iron deficiency response, as both responses are associated with the production and secretion of coumarins. Coumarins can mobilize iron from the soil environment and have a selective antimicrobial activity that impacts microbiome assembly in the rhizosphere. Being highly coumarin-tolerant, WCS417 induces the secretion of these phenolic compounds, likely to improve its own niche establishment, while providing growth and immunity benefits for the host in return. To investigate the possible signaling function of coumarins in the mutualistic Arabidopsis-WCS417 interaction, we analyzed the transcriptome of WCS417 growing in root exudates of coumarin-producing Arabidopsis Col-0 and the coumarin-biosynthesis mutant f6′h1. We found that coumarins in F6′H1-dependent root exudates significantly affected the expression of 439 bacterial genes (8% of the bacterial genome). Of those, genes with functions related to transport and metabolism of carbohydrates, amino acids, and nucleotides were induced, whereas genes with functions related to cell motility, the bacterial mobilome, and energy production and conversion were repressed. Strikingly, most genes related to flagellar biosynthesis were down-regulated by F6′H1-dependent root exudates and we found that application of selected coumarins reduces bacterial motility. These findings suggest that coumarins’ function in the rhizosphere as semiochemicals in the communication between the roots and WCS417. Collectively, our results provide important novel leads for future functional analysis of molecular processes in the establishment of plant-mutualist interactions.