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Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions.In this Review, Trivedi and colleagues explore the interactions between plants, their associated microbial communities and the environment, and also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.

A global assessment of the structure and function of the crop microbiome is urgently needed for the development of effective and rationally designed microbiome technologies for sustainable agriculture. Such an effort will provide new knowledge on the key ecological and evolutionary interactions between plant species and their microbiomes that can be harnessed for increasing agriculture productivity.

• An emerging experimental framework suggests that plants under biotic stress may actively seek help from soil microbes, but empirical evidence underlying such a ‘cry for help’ strategy is limited. • We used integrated microbial community profiling, pathogen and plant transcriptive gene quantification and culture-based methods to systematically investigate a three-way interaction between the wheat plant, wheat-associated microbiomes and Fusarium pseudograminearum (Fp). • A clear enrichment of a dominant bacterium, Stenotrophomonas rhizophila (SR80), was observed in both the rhizosphere and root endosphere of Fp-infected wheat. SR80 reached 3.7 × 10⁷ cells g−1 in the rhizosphere and accounted for up to 11.4% of the microbes in the root endosphere. Its abundance had a positive linear correlation with the pathogen load at base stems and expression of multiple defence genes in top leaves. Upon re-introduction in soils, SR80 enhanced plant growth, both the below-ground and above-ground, and induced strong disease resistance by boosting plant defence in the above-ground plant parts, but only when the pathogen was present. • Together, the bacterium SR80 seems to have acted as an early warning system for plant defence. This work provides novel evidence for the potential protection of plants against pathogens by an enriched beneficial microbe via modulation of the plant immune system.

Despite having key functions in terrestrial ecosystems, information on the dominant soil fungi and their ecological preferences at the global scale is lacking. To fill this knowledge gap, we surveyed 235 soils from across the globe. Our findings indicate that 83 phylotypes (<0.1% of the retrieved fungi), mostly belonging to wind dispersed, generalist Ascomycota, dominate soils globally. We identify patterns and ecological drivers of dominant soil fungal taxa occurrence, and present a map of their distribution in soils worldwide. Whole-genome comparisons with less dominant, generalist fungi point at a significantly higher number of genes related to stress-tolerance and resource uptake in the dominant fungi, suggesting that they might be better in colonising a wide range of environments. Our findings constitute a major advance in our understanding of the ecology of fungi, and have implications for the development of strategies to preserve them and the ecosystem functions they provide. Soil fungi play essential roles in ecosystems worldwide. Here, the authors sequence and analyze 235 soil samples collected from across the globe, and identify dominant fungal taxa and their associated environmental attributes.

Summary The use of microbial tools to sustainably increase agricultural production has received significant attention from researchers, industries and policymakers. Over the past decade, the market access and development of microbial products have been accelerated by (i) the recent advances in plant‐associated microbiome science, (ii) the pressure from consumers and policymakers for increasing crop productivity and reducing the use of agrochemicals, (iii) the rising threats of biotic and abiotic stresses, (iv) the loss of efficacy of some agrochemicals and plant breeding programs and (v) the calls for agriculture to contribute towards mitigating climate change. Although the sector is still in its infancy, the path towards effective microbial products is taking shape and the global market of these products has increased faster than that of agrochemicals. Promising results from using microbes either as biofertilizers or biopesticides have been continually reported, fuelling optimism and high expectations for the sector. However, some limitations, often related to low efficacy and inconsistent performance in field conditions, urgently need to be addressed to promote a wider use of microbial tools. We propose that advances in in situ microbiome manipulation approaches, such as the use of products containing synthetic microbial communities and novel prebiotics, have great potential to overcome some of these current constraints. Much more progress is expected in the development of microbial inoculants as areas such as synthetic biology and nano‐biotechnology advance. If key technical, translational and regulatory issues are addressed, microbial tools will not only play an important role in sustainably boosting agricultural production over the next few decades but also contribute towards other sustainable development goals, including job creation and mitigation of the impacts of climate change. Advances in in situ microbiome manipulation approaches, such as the use of products containing synthetic microbial communities and novel prebiotics, have the potential to overcome major limitations in the development of microbial tools in agriculture. Much more progress is expected in the development of microbial inoculants as areas such as synthetic biology and nano‐biotechnology advance.

Soil bacteria play key roles in regulating terrestrial carbon dynamics, nutrient cycles, and plant productivity. However, the natural histories and distributions of these organisms remain largely undocumented. Delgado-Baquerizo et al. provide a survey of the dominant bacterial taxa found around the world. In soil collections from six continents, they found that only 2% of bacterial taxa account for nearly half of the soil bacterial communities across the globe. These dominant taxa could be clustered into ecological groups of co-occurring bacteria that share habitat preferences. The findings will allow for a more predictive understanding of soil bacterial diversity and distribution. Science , this issue p. 320 Relatively few soil bacterial taxa dominate terrestrial ecosystems worldwide, with predictable distributions and ecology. The immense diversity of soil bacterial communities has stymied efforts to characterize individual taxa and document their global distributions. We analyzed soils from 237 locations across six continents and found that only 2% of bacterial phylotypes (~500 phylotypes) consistently accounted for almost half of the soil bacterial communities worldwide. Despite the overwhelming diversity of bacterial communities, relatively few bacterial taxa are abundant in soils globally. We clustered these dominant taxa into ecological groups to build the first global atlas of soil bacterial taxa. Our study narrows down the immense number of bacterial taxa to a “most wanted” list that will be fruitful targets for genomic and cultivation-based efforts aimed at improving our understanding of soil microbes and their contributions to ecosystem functioning.

Harnessing the plant microbiome therefore can potentially revolutionize agriculture and food industries by (i) integrating crop health with better management practices for specific climatic conditions to improve productivity and quality; (ii) using environmental friendly approaches to control pests and pathogens and thus reduce the use of chemical pesticides with environmental and health implications; (iii) considering smarter and efficient methods for using natural resources including soil and water; (iv) producing a better quality of food with less chemical contamination and allergens; and (v) minimizing losses by improving crop fitness in extreme weather or future change scenarios. [...]this may not be true in all cases and may be crop‐, region‐ and climate‐specific. [...]we firstly need a complete characterization of the phytomicrobiome associated with crop varieties and different compartments (e.g. leaf, stem, root) grown under different environmental and climatic conditions. Excessive use of agrochemicals has also negatively impacted the strength of this relationship. [...]future breeding programmes will need to use a combination of genetic information from the host and metabolic pathways from the associated microbiomes. Crop and soil microbiomes are a core component of this initiative and are working closely with the Phytobiome initiative to ensure success. (ii) The EU Commission has launched the International Bioeconomy Forum (IBF) on 13 October 2016, and harnessing microbiomes for food and nutritional security is their first and key component, along with regional economic growth and job creation.

Despite the importance of microbial communities for ecosystem services and human welfare, the relationship between microbial diversity and multiple ecosystem functions and services (that is, multifunctionality) at the global scale has yet to be evaluated. Here we use two independent, large-scale databases with contrasting geographic coverage (from 78 global drylands and from 179 locations across Scotland, respectively), and report that soil microbial diversity positively relates to multifunctionality in terrestrial ecosystems. The direct positive effects of microbial diversity were maintained even when accounting simultaneously for multiple multifunctionality drivers (climate, soil abiotic factors and spatial predictors). Our findings provide empirical evidence that any loss in microbial diversity will likely reduce multifunctionality, negatively impacting the provision of services such as climate regulation, soil fertility and food and fibre production by terrestrial ecosystems. The role of microbial diversity in ecosystems is less well understood than, for example, that of plant diversity. Analysing two independent data sets at a global and regional scale, Delgado-Baquerizo et al . show positive effects of soil diversity on multiple terrestrial ecosystem functions.

Prebiotics are compounds that selectively stimulate the growth and activity of beneficial microorganisms. The use of prebiotics is a well-established strategy for managing human gut health. This concept can also be extended to plants where plant rhizosphere microbiomes can improve the nutrient acquisition and disease resistance. However, we lack effective strategies for choosing metabolites to elicit the desired impacts on plant health. In this study, we target the rhizosphere of tomato ( Solanum lycopersicum ) suffering from wilt disease (caused by Ralstonia solanacearum ) as source for potential prebiotic metabolites. We identify metabolites (ribose, lactic acid, xylose, mannose, maltose, gluconolactone, and ribitol) exclusively used by soil commensal bacteria (not positively correlated with R . solanacearum ) but not efficiently used by the pathogen in vitro. Metabolites application in the soil with 1 µmol g −1 soil effectively protects tomato and other Solanaceae crops, pepper ( Capsicum annuum ) and eggplant ( Solanum melongena ), from pathogen invasion. After adding prebiotics, the rhizosphere soil microbiome exhibits enrichment of pathways related to carbon metabolism and autotoxin degradation, which were driven by commensal microbes. Collectively, we propose a novel pathway for mining metabolites from the rhizosphere soil and their use as prebiotics to help control soil-borne bacterial wilt diseases. Prebiotics can be used to encourage beneficial organisms. Here, the authors select rhizosphere metabolites that can be used as prebiotics to reduce the effect of the plant pathogen Ralstonia .

A lack of empirical evidence for the microbial regulation of ecosystem processes, including carbon (C) degradation, hinders our ability to develop a framework to directly incorporate the genetic composition of microbial communities in the enzyme-driven Earth system models. Herein we evaluated the linkage between microbial functional genes and extracellular enzyme activity in soil samples collected across three geographical regions of Australia. We found a strong relationship between different functional genes and their corresponding enzyme activities. This relationship was maintained after considering microbial community structure, total C and soil pH using structural equation modelling. Results showed that the variations in the activity of enzymes involved in C degradation were predicted by the functional gene abundance of the soil microbial community ( R 2 >0.90 in all cases). Our findings provide a strong framework for improved predictions on soil C dynamics that could be achieved by adopting a gene-centric approach incorporating the abundance of functional genes into process models.