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Root exudates contain specialised metabolites that shape the plant's root microbiome. How host-specific microbes cope with these bioactive compounds, and how this ability affects root microbiomes, remains largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound in the maize rhizosphere MBOA (6-methoxybenzoxazolin-2(3H)-one) and formed AMPO (2-amino-7-methoxy-phenoxazin-3-one). AMPO forming bacteria were enriched in the rhizosphere of benzoxazinoid-producing maize and could use MBOA as carbon source. We identified a gene cluster associated with AMPO formation in microbacteria. The first gene in this cluster, bxdA encodes a lactonase that converts MBOA to AMPO in vitro. A deletion mutant of the homologous bxdA genes in the genus Sphingobium, did not form AMPO nor was it able to use MBOA as a carbon source. BxdA was identified in different genera of maize root bacteria. Here we show that plant-specialised metabolites select for metabolisation-competent root bacteria. BxdA represents a benzoxazinoid metabolisation gene whose carriers successfully colonize the maize rhizosphere and thereby shape the plant's chemical environmental footprint.
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Benzoxazinas , Raíces de Plantas , Rizosfera , Zea mays , Zea mays/microbiología , Benzoxazinas/metabolismo , Raíces de Plantas/microbiología , Raíces de Plantas/metabolismo , Proteínas Bacterianas/metabolismo , Proteínas Bacterianas/genética , Familia de Multigenes , Microbiota/genética , Microbiología del Suelo , Sphingomonadaceae/genética , Sphingomonadaceae/metabolismo , Sphingomonadaceae/enzimologíaRESUMEN
Plant microbiome interactions are bidirectional with processes leading to microbiome assembly and processes leading to effects on plants, so called microbiome feedbacks. With belowground focus we systematically decomposed both of these directions into plant and (root and rhizosphere) microbiome components to identify methodological challenges and research priorities. We found that the bidirectionality of plant microbiome interactions presents a challenge for genetic studies. Establishing causality is particularly difficult when a plant mutant has both, an altered phenotype and an altered microbiome. Is the mutation directly affecting the microbiome (e.g., through root exudates), which then causes an altered phenotype of the plant and/or is the altered microbiome the consequence of the mutation altering the plant's phenotype (e.g., root architecture)? Here, we put forward that feedback experiments allow to separate cause and effect and furthermore, they are useful for investigating plant interactions with complex microbiomes in natural soils. They especially allow to investigate the plant genetic basis how plants respond to soil microbiomes and we stress that such microbiome feedbacks are understudied compared to the mechanisms contributing to microbiome assembly. Thinking towards application, this may allow to develop crops with both abilities to assemble a beneficial microbiome and to actively exploit its feedbacks.
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Microbiota , Rizosfera , Microbiología del Suelo , Raíces de Plantas/microbiología , Raíces de Plantas/genética , Plantas/microbiología , Plantas/genéticaRESUMEN
The plant health status is determined by the interplay of plant-pathogen-microbiota in the rhizosphere. Here, we investigate this tripartite system focusing on the pathogen Fusarium oxysporum f. sp. lycopersici (FOL) and tomato plants as a model system. First, we explore differences in tomato genotype resistance to FOL potentially associated with the differential recruitment of plant-protective rhizosphere taxa. Second, we show the production of fusaric acid by FOL to trigger systemic changes in the rhizosphere microbiota. Specifically, we show this molecule to have opposite effects on the recruitment of rhizosphere disease-suppressive taxa in the resistant and susceptible genotypes. Last, we elucidate that FOL and fusaric acid induce changes in the tomato root exudation with direct effects on the recruitment of specific disease-suppressive taxa. Our study unravels a mechanism mediating plant rhizosphere assembly and disease suppression by integrating plant physiological responses to microbial-mediated mechanisms in the rhizosphere.
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Ácido Fusárico , Fusarium , Microbiota , Enfermedades de las Plantas , Exudados de Plantas , Raíces de Plantas , Rizosfera , Solanum lycopersicum , Ácido Fusárico/metabolismo , Fusarium/patogenicidad , Raíces de Plantas/microbiología , Raíces de Plantas/metabolismo , Solanum lycopersicum/microbiología , Solanum lycopersicum/metabolismo , Enfermedades de las Plantas/microbiología , Exudados de Plantas/metabolismo , Microbiología del Suelo , Resistencia a la Enfermedad , GenotipoRESUMEN
By releasing specialized metabolites, plants modify their environment. Whether and how specialized metabolites protect plants against toxic levels of trace elements is not well understood. We evaluated whether benzoxazinoids, which are released into the soil by major cereals, can confer protection against arsenic toxicity. Benzoxazinoid-producing maize plants performed better in arsenic-contaminated soils than benzoxazinoid-deficient mutants in the greenhouse and the field. Adding benzoxazinoids to the soil restored the protective effect, and the effect persisted to the next crop generation via positive plant-soil feedback. Arsenate levels in the soil and total arsenic levels in the roots were lower in the presence of benzoxazinoids. Thus, the protective effect of benzoxazinoids is likely soil-mediated and includes changes in soil arsenic speciation and root accumulation. We conclude that exuded specialized metabolites can enhance protection against toxic trace elements via soil-mediated processes and may thereby stabilize crop productivity in polluted agroecosystems.
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Arsénico , Contaminantes del Suelo , Oligoelementos , Arsénico/metabolismo , Oligoelementos/metabolismo , Zea mays/genética , Zea mays/metabolismo , Benzoxazinas/metabolismo , Plantas/metabolismo , Suelo , Contaminantes del Suelo/análisis , Raíces de Plantas/metabolismoRESUMEN
Alternative solutions to mineral fertilizers and pesticides that reduce the environmental impact of agriculture are urgently needed. Arbuscular mycorrhizal fungi (AMF) can enhance plant nutrient uptake and reduce plant stress; yet, large-scale field inoculation trials with AMF are missing, and so far, results remain unpredictable. We conducted on-farm experiments in 54 fields in Switzerland and quantified the effects on maize growth. Growth response to AMF inoculation was highly variable, ranging from -12% to +40%. With few soil parameters and mainly soil microbiome indicators, we could successfully predict 86% of the variation in plant growth response to inoculation. The abundance of pathogenic fungi, rather than nutrient availability, best predicted (33%) AMF inoculation success. Our results indicate that soil microbiome indicators offer a sustainable biotechnological perspective to predict inoculation success at the beginning of the growing season. This predictability increases the profitability of microbiome engineering as a tool for sustainable agricultural management.
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Microbiota , Micorrizas , Micorrizas/fisiología , Suelo , Raíces de Plantas/microbiología , Agricultura/métodosRESUMEN
Plants exude specialized metabolites from their roots, and these compounds are known to structure the root microbiome. However, the underlying mechanisms are poorly understood. We established a representative collection of maize root bacteria and tested their tolerance against benzoxazinoids (BXs), the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that BXs inhibited bacterial growth in a strain- and compound-dependent manner. Tolerance against these selective antimicrobial compounds depended on bacterial cell wall structure. Further, we found that native root bacteria isolated from maize tolerated the BXs better compared to nonhost Arabidopsis bacteria. This finding suggests the adaptation of the root bacteria to the specialized metabolites of their host plant. Bacterial tolerance to 6-methoxy-benzoxazolin-2-one (MBOA), the most abundant and selective antimicrobial metabolite in the maize rhizosphere, correlated significantly with the abundance of these bacteria on BX-exuding maize roots. Thus, strain-dependent tolerance to BXs largely explained the abundance pattern of bacteria on maize roots. Abundant bacteria generally tolerated MBOA, while low abundant root microbiome members were sensitive to this compound. Our findings reveal that tolerance to plant specialized metabolites is an important competence determinant for root colonization. We propose that bacterial tolerance to root-derived antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities.
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Antiinfecciosos , Arabidopsis , Microbiota , Zea mays/metabolismo , Raíces de Plantas/metabolismo , Bacterias/metabolismo , Plantas/metabolismo , Rizosfera , Benzoxazinas/farmacología , Benzoxazinas/metabolismo , Arabidopsis/metabolismo , Antiinfecciosos/metabolismo , Microbiología del SueloRESUMEN
Plant secondary metabolites that are released into the rhizosphere alter biotic and abiotic soil properties, which in turn affect the performance of other plants. How this type of plant-soil feedback affects agricultural productivity and food quality in the field in the context of crop rotations is unknown. Here, we assessed the performance, yield and food quality of three winter wheat varieties growing in field plots whose soils had been conditioned by either wild type or benzoxazinoid-deficient bx1 maize mutant plants. Following maize cultivation, we detected benzoxazinoid-dependent chemical and microbial fingerprints in the soil. The benzoxazinoid fingerprint was still visible during wheat growth, but the microbial fingerprint was no longer detected. Wheat emergence, tillering, growth, and biomass increased in wild type conditioned soils compared to bx1 mutant conditioned soils. Weed cover was similar between soil conditioning treatments, but insect herbivore abundance decreased in benzoxazinoid-conditioned soils. Wheat yield was increased by over 4% without a reduction in grain quality in benzoxazinoid-conditioned soils. This improvement was directly associated with increased germination and tillering. Taken together, our experiments provide evidence that soil conditioning by plant secondary metabolite producing plants can increase yield via plant-soil feedbacks under agronomically realistic conditions. If this phenomenon holds true across different soils and environments, optimizing root exudation chemistry could be a powerful, genetically tractable strategy to enhance crop yields without additional inputs.
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Benzoxazinas , Suelo , Suelo/química , Retroalimentación , Benzoxazinas/metabolismo , Agricultura , Zea mays/metabolismo , Grano Comestible/metabolismo , TriticumRESUMEN
BACKGROUND: A major aim in plant microbiome research is determining the drivers of plant-associated microbial communities. While soil characteristics and host plant identity present key drivers of root microbiome composition, it is still unresolved whether the presence or absence of important plant root symbionts also determines overall microbiome composition. Arbuscular mycorrhizal fungi (AMF) and N-fixing rhizobia bacteria are widespread, beneficial root symbionts that significantly enhance plant nutrition, plant health, and root structure. Thus, we hypothesized that symbiont types define the root microbiome structure. RESULTS: We grew 17 plant species from five families differing in their symbiotic associations (no symbioses, AMF only, rhizobia only, or AMF and rhizobia) in a greenhouse and used bacterial and fungal amplicon sequencing to characterize their root microbiomes. Although plant phylogeny and species identity were the most important factors determining root microbiome composition, we discovered that the type of symbioses also presented a significant driver of diversity and community composition. We found consistent responses of bacterial phyla, including members of the Acidobacteria, Chlamydiae, Firmicutes, and Verrucomicrobia, to the presence or absence of AMF and rhizobia and identified communities of OTUs specifically enriched in the different symbiotic groups. A total of 80, 75 and 57 bacterial OTUs were specific for plant species without symbiosis, plant species forming associations with AMF or plant species associating with both AMF and rhizobia, respectively. Similarly, 9, 14 and 4 fungal OTUs were specific for these plant symbiont groups. Importantly, these generic symbiosis footprints in microbial community composition were also apparent in absence of the primary symbionts. CONCLUSION: Our results reveal that symbiotic associations of the host plant leaves an imprint on the wider root microbiome - which we term the symbiotype. These findings suggest the existence of a fundamental assembly principle of root microbiomes, dependent on the symbiotic associations of the host plant.
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Zinc (Zn) is an important micronutrient but can be toxic at elevated concentrations. We conducted an experiment to test the effect of plant growth and soil microbial disturbance on Zn in soil and plants. Pots were prepared with and without maize and in an undisturbed soil, a soil that was disturbed by X-ray sterilization and a soil that was sterilized but reconditioned with the original microbiome. The Zn concentration and isotope fractionation between the soil and the soil pore water increased with time, which is probably due to physical disturbance and fertilization. The presence of maize increased the Zn concentration and isotope fractionation in pore water. This was likely related to the uptake of light isotopes by plants and root exudates that solubilized heavy Zn from the soil. The sterilization disturbance increased the concentration of Zn in the pore water, because of abiotic and biotic changes. Despite a threefold increase in Zn concentration and changes in the Zn isotope composition in the pore water, the Zn content and isotope fractionation in the plant did not change. These results have implications for Zn mobility and uptake in crop plants and are relevant in terms of Zn nutrition.
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Contaminantes del Suelo , Suelo , Suelo/química , Isótopos de Zinc/química , Zinc/química , Isótopos , Plantas , Raíces de PlantasRESUMEN
We carried out a 4-year manipulative field experiment in a semiarid shrubland in southeastern Spain to assess the impacts of experimental warming (W), rainfall reduction (RR), and their combination (W + RR) on the composition and diversity of arbuscular mycorrhizal fungal (AMF) communities in rhizosphere soil of H. syriacum and G. struthium shrubs using single-molecule real-time (SMRT) DNA sequencing. Across climate treatments, we encountered 109 AMF operational taxonomic units (OTUs) that were assigned to four families: Glomeraceae (93.94%), Gigasporaceae (2.19%), Claroideoglomeraceae (1.95%), and Diversisporaceae (1.92%). AMF community composition and diversity at OTU level were unaffected by the climate manipulation treatments, except for a significant decrease in AMF OTU richness in the W treatment relative to the control. However, we found a significant decrease of AMF family richness in all climate manipulation treatments relative to the control treatment. Members of the Gigasporaceae and Diversisporaceae families appeared to be highly vulnerable to intensification of heat and drought stress, as their abundances decreased by 67% and 77%, respectively, in the W + RR treatment relative to current ambient conditions. In contrast, the relative abundance and dominance of the Glomeraceae family within the AMF community increased significantly under the W + RR treatment, with Glomeraceae being the indicator family for the W + RR treatment. The interaction between warming and rainfall reduction had a significant effect on AMF community structure at family level. These findings provide new insights to help in the conservation of the soil biodiversity facing climate change in dryland ecosystems.
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Glomeromycota , Micorrizas , Humanos , Micorrizas/genética , Ecosistema , Microbiología del Suelo , Biodiversidad , Suelo/química , Raíces de Plantas/microbiologíaRESUMEN
Root-microbiome interactions are of central importance for plant performance and yield. A distinctive feature of legumes is that they engage in symbiosis with N2-fixing rhizobia. If and how the rhizobial symbiotic capacity modulates root-associated microbiomes are still not yet well understood. We determined root-associated microbiomes of soybean inoculated with wild type (WT) or a noeI mutant of Bradyrhizobium diazoefficiens USDA 110 by amplicon sequencing. UPLC-MS/MS was used to analyze root exudates. The noeI gene is responsible for fucose-methylation of Nod factor secreted by USDA 110 WT strain. Soybean roots inoculated with the noeI mutant showed a significant decrease in nodulation and root-flavonoid exudation compared to roots inoculated with WT strain. The noeI mutant-inoculated roots exhibited strong changes in microbiome assembly in the rhizosphere and rhizoplane, including reduced diversity, changed co-occurrence interactions and a substantial depletion of root microbes. Root exudates and soil physiochemical properties were significantly correlated with microbial community shift in the rhizosphere between different rhizobial treatments. These results illustrate that rhizobial symbiotic capacity dramatically alters root-associated microbiomes, in which root exudation and edaphic patterns play a vital role. This study has important implications for understanding the evolution of plant-microbiome interactions.
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Plant-soil feedbacks refer to effects on plants that are mediated by soil modifications caused by the previous plant generation. Maize conditions the surrounding soil by secretion of root exudates including benzoxazinoids (BXs), a class of bioactive secondary metabolites. Previous work found that a BX-conditioned soil microbiota enhances insect resistance while reducing biomass in the next generation of maize plants. Whether these BX-mediated and microbially driven feedbacks are conserved across different soils and response species is unknown. We found the BX-feedbacks on maize growth and insect resistance conserved between two arable soils, but absent in a more fertile grassland soil, suggesting a soil-type dependence of BX feedbacks. We demonstrated that wheat also responded to BX-feedbacks. While the negative growth response to BX-conditioning was conserved in both cereals, insect resistance showed opposite patterns, with an increase in maize and a decrease in wheat. Wheat pathogen resistance was not affected. Finally and consistent with maize, we found the BX-feedbacks to be cultivar-specific. Taken together, BX-feedbacks affected cereal growth and resistance in a soil and genotype-dependent manner. Cultivar-specificity of BX-feedbacks is a key finding, as it hides the potential to optimize crops that avoid negative plant-soil feedbacks in rotations.
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Alelopatía , Benzoxazinas/metabolismo , Genotipo , Suelo/química , Triticum/fisiología , Zea mays/fisiología , Animales , Cadena Alimentaria , Insectos/fisiología , Triticum/genética , Zea mays/genéticaRESUMEN
The aboveground impacts of climate change receive extensive research attention, but climate change could also alter belowground processes such as the delicate balance between free-living fungal decomposers and nutrient-scavenging mycorrhizal fungi that can inhibit decomposition through a mechanism called the Gadgil effect. We investigated how climate change-induced reductions in plant survival, photosynthesis and productivity alter soil fungal community composition in a mixed arbuscular/ectomycorrhizal (AM/EM) semiarid shrubland exposed to experimental warming (W) and/or rainfall reduction (RR). We hypothesised that increased EM host plant mortality under a warmer and drier climate might decrease ectomycorrhizal fungal (EMF) abundance, thereby favouring the proliferation and activity of fungal saprotrophs. The relative abundance of EMF sequences decreased by 57.5% under W+RR, which was accompanied by reductions in the activity of hydrolytic enzymes involved in the acquisition of organic-bound nutrients by EMF and their host plants. W+RR thereby created an enhanced potential for soil organic matter (SOM) breakdown and nitrogen mineralisation by decomposers, as revealed by 127-190% increases in dissolved organic carbon and nitrogen, respectively, and decreasing SOM content in soil. Climate aridification impacts on vegetation can cascade belowground through shifts in fungal guild structure that alter ecosystem biogeochemistry and accelerate SOM decomposition by reducing the Gadgil effect.
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Micorrizas , Carbono , Ecosistema , Hongos , Nitrógeno , Suelo , Microbiología del SueloRESUMEN
Ecosystems provide multiple services to humans. However, agricultural systems are usually evaluated on their productivity and economic performance, and a systematic and quantitative assessment of the multifunctionality of agroecosystems including environmental services is missing. Using a long-term farming system experiment, we evaluated and compared the agronomic, economic, and ecological performance of the most widespread arable cropping systems in Europe: organic, conservation, and conventional agriculture. We analyzed 43 agroecosystem properties and determined overall agroecosystem multifunctionality. We show that organic and conservation agriculture promoted ecosystem multifunctionality, especially by enhancing regulating and supporting services, including biodiversity preservation, soil and water quality, and climate mitigation. In contrast, conventional cropping showed reduced multifunctionality but delivered highest yield. Organic production resulted in higher economic performance, thanks to higher product prices and additional support payments. Our results demonstrate that different cropping systems provide opposing services, enforcing the productivity-environmental protection dilemma for agroecosystem functioning.
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BACKGROUND: Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties. RESULTS: Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments. CONCLUSIONS: These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions. Video Abstract.
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Microbiota , Zea mays , Benzoxazinas , Europa (Continente) , Microbiota/genética , Fitomejoramiento , Raíces de Plantas , Rizosfera , Microbiología del SueloRESUMEN
Plants are systemically relevant to our planet not only by constituting a major part of its biomass, but also because they produce a vast diversity of bioactive phytochemicals. These compounds often modulate interactions between plants and the environment, and can have substantial effects on plant consumers and their health. By taking a food web perspective, we highlight the role of bioactive phytochemicals in linking soils, plants, animals and humans and discuss their contributions to systems health. The analysis of connections among food web components revealed an underexplored potential of phytochemicals to optimize food web health and productivity.
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Cadena Alimentaria , Fitoquímicos , Animales , PlantasRESUMEN
Arbuscular mycorrhiza fungi (AMF) are beneficial soil fungi that can promote the growth of their host plants. Accurate quantification of AMF in plant roots is important because the level of colonization is often indicative of the activity of these fungi. Root colonization is traditionally measured with microscopy methods which visualize fungal structures inside roots. Microscopy methods are labor-intensive, and results depend on the observer. In this study, we present a relative qPCR method to quantify AMF in which we normalized the AMF qPCR signal relative to a plant gene. First, we validated the primer pair AMG1F and AM1 in silico, and we show that these primers cover most AMF species present in plant roots without amplifying host DNA. Next, we compared the relative qPCR method with traditional microscopy based on a greenhouse experiment with Petunia plants that ranged from very high to very low levels of AMF root colonization. Finally, by sequencing the qPCR amplicons with MiSeq, we experimentally confirmed that the primer pair excludes plant DNA while amplifying mostly AMF. Most importantly, our relative qPCR approach was capable of discriminating quantitative differences in AMF root colonization and it strongly correlated (Spearman Rho = 0.875) with quantifications by traditional microscopy. Finally, we provide a balanced discussion about the strengths and weaknesses of microscopy and qPCR methods. In conclusion, the tested approach of relative qPCR presents a reliable alternative method to quantify AMF root colonization that is less operator-dependent than traditional microscopy and offers scalability to high-throughput analyses.
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Micorrizas , Hongos , Micorrizas/genética , Raíces de Plantas , Plantas , Suelo , Microbiología del SueloRESUMEN
The miCROPe 2019 symposium, which took place from 2 to 5 December 2019 in Vienna, Austria, has unified researchers and industry from around the world to discuss opportunities, challenges and needs of microbe-assisted crop production. There is broad consensus that microorganisms-with their abilities to alleviate biotic and abiotic stresses and to improve plant nutrition-offer countless opportunities to enhance plant productivity and to ameliorate agricultural sustainability. However, microbe-assisted cultivation approaches face challenges that need to be addressed before a breakthrough of such technologies can be expected. Following up on the miCROPe symposium and a linked satellite workshop on breeding for beneficial plant-microbe interactions, we carved out research priorities towards successful implementation of microbiome knowledge for modern agriculture. These include (i) to solve context dependency for microbial inoculation approaches and (ii) to identify the genetic determinants to allow breeding for beneficial plant-microbiome interactions. With the combination of emerging third generation sequencing technologies and new causal research approaches, we now stand at the crossroad of utilising microbe-assisted crop production as a reliable and sustainable agronomic practice.