The rhizosphere, the thin layer of soil surrounding and influenced by plant roots, defines a distinct and selective microbial habitat compared to unplanted soil. The microbial communities inhabiting the rhizosphere, the rhizosphere microbiota, engage in interactions with their host plants which span from parasitism to mutualism. Therefore, the rhizosphere microbiota emerges as one of the determinants of yield potential in crops. Studies conducted with different plant species have unequivocally pointed to the host plant as a driver of the microbiota thriving at the root–soil interface. Thus far, the host genetic traits shaping the rhizosphere microbiota are not completely understood. As root hairs play a critical role in resource exchanges between plants and the rhizosphere, we hypothesized that they can act as a determinant of the microbiota thriving at the root–soil interface. To test this hypothesis, we took advantage of barley (Hordeum vulgare) mutant lines contrasting for their root hair characteristics. Plants were grown in two agricultural soils, differentiating in their organic matter contents, under controlled environmental conditions. At early stem elongation rhizosphere specimens were collected and subjected to high-resolution 16S rRNA gene profiling. Our data revealed that the barley rhizosphere microbiota is largely dominated by members of the phyla Bacteroidetes and Proteobacteria, regardless of the soil type and the root hair characteristics of the host plant. Conversely, ecological indices calculated using operational taxonomic units (OTUs) presence, abundance, and phylogeny revealed a significant impact of root hair mutations on the composition of the rhizosphere microbiota. In particular, our data indicate that mutant plants host a reduced-complexity community compared to wild-type genotypes and unplanted soil controls. Congruently, the host genotype explained up to 18% of the variation in ecological distances computed for the rhizosphere samples. Importantly, this effect is manifested in a soil-dependent manner. A closer inspection of the sequencing profiles revealed that the root hair-dependent diversification of the microbiota is supported by a taxonomically narrow group of bacteria, with a bias for members of the orders Actinomycetales, Burkholderiales, Rhizobiales, Sphingomonadales, and Xanthomonadales. Taken together, our results indicate that the presence and function of root hairs are a determinant of the bacterial community thriving in the rhizosphere and their perturbations can markedly impact on the recruitment of individual members of the microbiota.
Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally reveal early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. Using RNA-sequencing, we show that these beneficial activities are not associated with extensive host transcriptional reprogramming but rather with the modulation of expression of microbial effectors and carbohydrate-active enzymes.
The microbial communities thriving at the root−soil interface have the potential to improve plant growth and sustainable crop production. Yet, how agricultural practices, such as the application of either mineral or organic nitrogen fertilizers, impact on the composition and functions of these communities remains to be fully elucidated. By deploying a two-pronged 16S rRNA gene sequencing and predictive metagenomics approach, we demonstrated that the bacterial microbiota of field-grown tomato (Solanum lycopersicum) plants is the product of a selective process that progressively differentiates between rhizosphere and root microhabitats. This process initiates as early as plants are in a nursery stage and it is then more marked at late developmental stages, in particular at harvest. This selection acts on both the bacterial relative abundances and phylogenetic assignments, with a bias for the enrichment of members of the phylum Actinobacteria in the root compartment. Digestate-based and mineral-based nitrogen fertilizers trigger a distinct bacterial enrichment in both rhizosphere and root microhabitats. This compositional diversification mirrors a predicted functional diversification of the root-inhabiting communities, manifested predominantly by the differential enrichment of genes associated to ABC transporters and the two-component system. Together, our data suggest that the microbiota thriving at the tomato root−soil interface is modulated by and in responses to the type of nitrogen fertilizer applied to the field. [Formula: see text] Copyright © 2019 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .
BackgroundSince the dawn of agriculture, human selection on plants has progressively differentiated input-demanding productive crops from their wild progenitors thriving in marginal areas. Barley (Hordeum vulgare), the fourth most cultivated cereal globally, is a prime example of this process. We previously demonstrated that wild and domesticated barley genotypes host distinct microbial communities in their rhizosphere. Here we tested the hypothesis that microbiota diversification is modulated by, and in response to, nitrogen (N) application in soil and we assessed the impact of microbiota composition on plant growth.MethodsWe grew two wild (H. vulgaressp.spontaneum) and a modern domesticated (H. vulgaressp.vulgare) barley genotypes in an agricultural soil amended with and without nitrogen (N) inputs. By using a two-pronged 16S rRNA gene survey and a shotgun metagenomics approach, we determined the impact of N application on the taxonomic composition of the barley microbiota as well as the functional diversification of microbial communities exposed to limiting nitrogen supplies. In parallel, we used metagenomics reads to reconstruct genomes of individual bacterial members of the microbiota. Finally, we implemented a plant-soil feedback experiment to assess the microbiota’s contribution to plant growth.ResultsRhizosphere profiles were distinct from unplanted soil controls and displayed a significant, plant-mediated, N application-dependent taxonomic diversification which is maximised under N-limiting conditions. Strikingly, this diversification mirrors a metabolic specialisation of the barley microbiota, with functions implicated in nitrogen and sulphur metabolism enriched in a wild genotype as opposed to the RNA and cell capsule metabolisms enriched in a modern genotype. We reconstruct 28 high-quality individual bacterial genomes with a bias for Bacteroidetes and Proteobacteria, which are among the taxa differentially recruited between wild and modern genotypes. A plant-soil feedback experiment revealed that modern plants exposed to heat-sterilised soils grew less compared to plants maintained in untreated soils, although this difference was significant only for plants exposed to the wild barley microbiota.ConclusionsOur results point at nitrogen availability as a modulator of the structural and functional configuration of the rhizosphere bacterial communities and suggest a limited, but significant, contribution of the wild barley microbiota to plant growth. This knowledge will contribute to devise strategies to enhance sustainable crop production.
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