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Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System.

ABSTRACT: Root-associated microbes are critical to plant health and performance, although understanding of the factors that structure these microbial communities and the theory to predict microbial assemblages are still limited. Here, we use a grafted tomato system to study the effects of rootstock genotypes and grafting in endosphere and rhizosphere microbiomes that were evaluated by sequencing 16S rRNA. We compared the microbiomes of nongrafted tomato cultivar BHN589, self-grafted BHN589, and BHN589 grafted to Maxifort or RST-04-106 hybrid rootstocks. Operational taxonomic unit (OTU)-based bacterial diversity was greater in Maxifort compared to the nongrafted control, whereas bacterial diversity in the controls (self-grafted and nongrafted) and the other rootstock (RST-04-106) was similar. Grafting itself did not affect bacterial diversity; diversity in the self-graft was similar to that of the nongraft. Bacterial diversity was higher in the rhizosphere than in the endosphere for all treatments. However, despite the lower overall diversity, there was a greater number of differentially abundant OTUs (DAOTUs) in the endosphere, with the greatest number of DAOTUs associated with Maxifort. In a permutational multivariate analysis of variance (PERMANOVA), there was evidence for an effect of rootstock genotype on bacterial communities. The endosphere-rhizosphere compartment and study site explained a high percentage of the differences among bacterial communities. Further analyses identified OTUs responsive to rootstock genotypes in both the endosphere and rhizosphere. Our findings highlight the effects of rootstocks on bacterial diversity and composition. The influence of rootstock and plant compartment on microbial communities indicates opportunities for the development of designer communities and microbiome-based breeding to improve future crop production.IMPORTANCE Understanding factors that control microbial communities is essential for designing and supporting microbiome-based agriculture. In this study, we used a grafted tomato system to study the effect of rootstock genotypes and grafting on bacterial communities colonizing the endosphere and rhizosphere. To compare the bacterial communities in control treatments (nongrafted and self-grafted plants) with the hybrid rootstocks used by farmers, we evaluated the effect of rootstocks on overall bacterial diversity and composition. These findings indicate the potential for using plant genotype to indirectly select bacterial taxa. In addition, we identify taxa responsive to each rootstock treatment, which may represent candidate taxa useful for biocontrol and in biofertilizers.

SUBMITTER: Poudel R

PROVIDER: S-EPMC6328775 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System.

Poudel Ravin R Jumpponen Ari A Kennelly Megan M MM Rivard Cary L CL Gomez-Montano Lorena L Garrett Karen A KA

Applied and environmental microbiology 20190109 2

Root-associated microbes are critical to plant health and performance, although understanding of the factors that structure these microbial communities and the theory to predict microbial assemblages are still limited. Here, we use a grafted tomato system to study the effects of rootstock genotypes and grafting in endosphere and rhizosphere microbiomes that were evaluated by sequencing 16S rRNA. We compared the microbiomes of nongrafted tomato cultivar BHN589, self-grafted BHN589, and BHN589 gra ...[more]

PMID: 30413478

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Project description:BackgroundWhile the rootstock genotype (belowground part of a plant) can impact rhizosphere microbial communities, few studies have examined the relationships between rootstock genotype-based recruitment of active rhizosphere bacterial communities and the availability of root nutrients for plant uptake. Rootstocks are developed to provide resistance to disease or tolerance of abiotic stresses, and compost application is a common practice to also control biotic and abiotic stresses in crops. In this field study, we examined: (i) the effect of four citrus rootstocks and/or compost application on the abundance, diversity, composition, and predicted functionality of active rhizosphere bacterial communities, and (ii) the relationships between active rhizosphere bacterial communities and root nutrient concentrations, with identification of bacterial taxa significantly correlated with changes in root nutrients in the rhizosphere.ResultsThe rootstock genotype determined differences in the diversity of active rhizosphere bacterial communities and also impacted how compost altered the abundance, diversity, composition, and predicted functions of these active communities. Variations in the active bacterial rhizobiome were strongly linked to root nutrient cycling, and these interactions were root-nutrient- and rootstock-specific. Direct positive relationships between enriched taxa in treated soils and specific root nutrients were detected, and potentially important taxa for root nutrient uptake were identified. Significant differences in specific predicted functions were related to soil nutrient cycling (carbon, nitrogen, and tryptophan metabolisms) in the active bacterial rhizobiome among rootstocks, particularly in soils treated with compost.ConclusionsThis study illustrates that interactions between citrus rootstocks and compost can influence active rhizosphere bacterial communities, which impact root nutrient concentrations. In particular, the response of the rhizobiome bacterial abundance, diversity, and community composition to compost was determined by the rootstock. Specific bacterial taxa therefore appear to be driving changes in root nutrient concentrations in the active rhizobiome of different citrus rootstocks. Several potential functions of active bacterial rhizobiomes recruited by different citrus rootstocks did not appear to be redundant but rather rootstock-specific. Together, these findings have important agronomic implications as they indicate the potential for agricultural production systems to maximize benefits from rhizobiomes through the choice of selected rootstocks and the application of compost. Video Abstract.

Project description:Microorganisms that colonize the plant rhizosphere can contribute to plant health, growth and productivity. Although the importance of the rhizosphere microbiome is known, we know little about the underlying mechanisms that drive microbiome assembly and composition. In this study, the variation, assembly and composition of rhizobacterial communities in 11 tomato cultivars, combined with one cultivar in seven different sources of soil and growing substrate, were systematically investigated. The tomato rhizosphere microbiota was dominated by bacteria from the phyla Proteobacteria, Bacteroidetes, and Acidobacteria, mainly comprising Rhizobiales, Xanthomonadales, Burkholderiales, Nitrosomonadales, Myxococcales, Sphingobacteriales, Cytophagales and Acidobacteria subgroups. The bacterial community in the rhizosphere microbiota of the samples in the cultivar experiment mostly overlapped with that of tomato cultivar MG, which was grown in five natural field soils, DM, JX, HQ, QS and XC. The results supported the hypothesis that tomato harbors largely conserved communities and compositions of rhizosphere microbiota that remains consistent in different cultivars of tomato and even in tomato cultivar grown in five natural field soils. However, significant differences in OTU richness (p < 0.0001) and bacterial diversity (p = 0.0014 < 0.01) were observed among the 7 different sources of soil and growing substrate. Two artificial commercial nutrient soils, HF and CF, resulted in a distinct tomato rhizosphere microbiota in terms of assembly and core community compared with that observed in natural field soils. PERMANOVA of beta diversity based on the combined data from the cultivar and soil experiments demonstrated that soil (growing substrate) and plant genotype (cultivar) had significant impacts on the rhizosphere microbial communities of tomato plants (soil, F = 22.29, R2 = 0.7399, p < 0.001; cultivar, F = 2.04, R2 = 0.3223, p = 0.008). Of these two factors, soil explained a larger proportion of the compositional variance in the tomato rhizosphere microbiota. The results demonstrated that the assembly process of rhizosphere bacterial communities was collectively influenced by soil, including the available bacterial sources and biochemical properties of the rhizosphere soils, and plant genotype.

Project description:Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory to Ferrovibrium and tested Firmicutes. While fungal isolates of Penicillium and Periconia were also more inhibited by higher concentrations (200 µM) of nerolidol, Clonostachys was enhanced at this higher level and together with Humicola was inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect on Orbilia at both tested concentrations but had a promotive effect at 100 µM on Penicillium and Periconia. Similarly, linalool at 100 µM had significant growth promotion in Mortierella, but an inhibitory effect for Orbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome. IMPORTANCE Terpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a "rhizobox" mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production.

Dataset Information

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System.

Publications

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System.

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