SummaryCrop disease outbreaks are often associated with clonal expansions of single pathogenic lineages. To determine whether similar boom-and-bust scenarios hold for wild pathosystems, we carried out a multi-year, multi-site survey of Pseudomonas in its natural host Arabidopsis thaliana. The most common Pseudomonas lineage corresponded to a ubiquitous pathogenic clade. Sequencing of 1,524 genomes revealed this lineage to have diversified approximately 300,000 years ago, containing dozens of genetically identifiable pathogenic sublineages. There is differentiation at the level of both gene content and disease phenotype, although the differentiation may not provide fitness advantages to specific sublineages. The coexistence of sublineages indicates that in contrast to crop systems, no single strain has been able to overtake the studied A. thaliana populations in the recent past. Our results suggest that selective pressures acting on a plant pathogen in wild hosts are likely to be much more complex than those in agricultural systems.

SignificanceMost terrestrial plants live in symbiosis with arbuscular mycorrhizal (AM) fungi and rely on this association to scavenge the macronutrient phosphorus (P) from soil. Arabis alpina thrives in P-limited alpine habitats, although, like all Brassicaceae species, it lacks the ability to establish an AM symbiosis. By studying the fungal microbiota associated with A. alpina roots we uncovered its association with a beneficial Helotiales fungus capable of promoting plant growth and P uptake, thereby facilitating plant adaptation to low-P environments.

Fluorescent pseudomonads protecting plant roots from phytopathogens by producing 2,4-diacetylphloroglucinol (DAPG) are considered to form a monophyletic lineage comprised of DAPG+ Pseudomonas strains in the “P. corrugata” and “P. protegens” subgroups of the “Pseudomonas fluorescens” group. However, DAPG production ability has not been investigated for many species of these two subgroups, and whether or not the DAPG+ Pseudomonas are truly monophyletic remained to be verified. Thus, the distribution of the DAPG biosynthetic operon (phlACBD genes) in the Pseudomonas spp. was investigated in sequenced genomes and type strains. Results showed that the DAPG+ Pseudomonas include species of the “P. fluorescens” group, i.e., P. protegens, P. brassicacearum, P. kilonensis, and P. thivervalensis, as expected, as well as P. gingeri in which it had not been documented. Surprisingly, they also include bacteria outside the “P. fluorescens” group, as exemplified by Pseudomonas sp. OT69, and even two Betaproteobacteria genera. The phl operon-based phylogenetic tree was substantially congruent with the one inferred from concatenated housekeeping genes rpoB, gyrB, and rrs. Contrariwise to current supposition, ancestral character reconstructions favored multiple independent acquisitions rather that one ancestral event followed by vertical inheritance. Indeed, based on synteny analyses, these acquisitions appeared to vary according to the Pseudomonas subgroup and even the phylogenetic groups within the subgroups. In conclusion, our study shows that the phl+ Pseudomonas populations form a polyphyletic group and suggests that DAPG biosynthesis might not be restricted to this genus. This is important to consider when assessing the ecological significance of phl+ bacterial populations in rhizosphere ecosystems.

Summary Plants respond to phosphorus (P) limitation through an array of morphological, physiological and metabolic changes which are part of the phosphate (Pi) starvation response ( PSR ). This response influences the establishment of the arbuscular mycorrhizal ( AM ) symbiosis in most land plants. It is, however, unknown to what extent available P and the PSR redefine plant interactions with the fungal microbiota in soil. Using amplicon sequencing of the fungal taxonomic marker ITS 2, we examined the changes in root‐associated fungal communities in the AM nonhost species Arabidopsis thaliana in response to soil amendment with P and to genetic perturbations in the plant PSR . We observed robust shifts in root‐associated fungal communities of P‐replete plants in comparison with their P‐deprived counterparts, while bulk soil communities remained unaltered. Moreover, plants carrying mutations in the phosphate signaling network genes, phr1 , phl1 and pho2 , exhibited similarly altered root fungal communities characterized by the depletion of the chytridiomycete taxon Olpidium brassicae specifically under P‐replete conditions. This study highlights the nutritional status and the underlying nutrient signaling network of an AM nonhost plant as previously unrecognized factors influencing the assembly of the plant fungal microbiota in response to P in nonsterile soil.

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SummarySoil suppressiveness to disease is an intriguing emerging property in agroecosystems, with important implications because it enables significant protection of susceptible plants from soil-borne pathogens. Unlike many soils where disease suppressiveness requires crop monoculture to establish, certain soils are naturally suppressive to disease, and this type of specific disease suppressiveness is maintained despite crop rotation. Soils naturally suppressive to Thielaviopsis basicola-mediated black root rot of tobacco and other crops occur in Morens region (Switzerland) and have been studied for over 30 years. In Morens, vermiculite-rich suppressive soils formed on morainic deposits while illite-rich conducive soils developed on sandstone, but suppressiveness is of microbial origin. Antagonistic pseudomonads play a role in black root rot suppressiveness, including Pseudomonas protegens (formerly P. fluorescens) CHA0, a major model strain for research. However, other types of rhizobacterial taxa may differ in prevalence between suppressive and conducive soils, suggesting that the microbial basis of black root rot suppressiveness could be far more complex than solely a Pseudomonas property. This first review on black root rot suppressive soils covers early findings on these soils, the significance of recent results, and compares them with other types of suppressive soils in terms of rhizosphere ecology and plant protection mechanisms.

Pseudomonas strains producing 2,4-diacetylphloroglucinol (DAPG) can protect plants from soilborne phytopathogens and are considered the primary reason for suppressiveness of morainic Swiss soils to Thielaviopsis basicola-mediated black root-rot disease of tobacco, even though they also occur nearby in conducive sandstone soils. The underlying molecular mechanisms accounting for this discrepancy are not understood. In this study, we assessed the hypothesis that the presence of iron-rich vermiculite clay (dominant in suppressive soils) instead of illite (dominant in neighboring conducive soils) translates into higher levels of iron bioavailability and transcription of Pseudomonas DAPG synthetic genes in the tobacco rhizosphere. Rhizosphere monitoring of reporter gene systems pvd-inaZ and phlA-gfp in Pseudomonas protegens indicated that the level of iron bioavailability and the number of cells expressing phl genes (DAPG synthesis), respectively, were higher in vermiculitic than in illitic artificial soils. This was in accordance with the effect of iron on phlA-gfp expression in vitro and, indeed, iron addition to the illitic soil increased the number of cells expressing phlA-gfp. Similar findings were made in the presence of the pathogen T. basicola. Altogether, results substantiate the hypothesis that iron-releasing minerals may confer disease suppressiveness by modulating iron bioavailability in the rhizosphere and expression of biocontrol-relevant genes in antagonistic P. protegens.