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Rhizosphere microbiome assemblage is affected by plant development.

ABSTRACT: There is a concerted understanding of the ability of root exudates to influence the structure of rhizosphere microbial communities. However, our knowledge of the connection between plant development, root exudation and microbiome assemblage is limited. Here, we analyzed the structure of the rhizospheric bacterial community associated with Arabidopsis at four time points corresponding to distinct stages of plant development: seedling, vegetative, bolting and flowering. Overall, there were no significant differences in bacterial community structure, but we observed that the microbial community at the seedling stage was distinct from the other developmental time points. At a closer level, phylum such as Acidobacteria, Actinobacteria, Bacteroidetes, Cyanobacteria and specific genera within those phyla followed distinct patterns associated with plant development and root exudation. These results suggested that the plant can select a subset of microbes at different stages of development, presumably for specific functions. Accordingly, metatranscriptomics analysis of the rhizosphere microbiome revealed that 81 unique transcripts were significantly (P<0.05) expressed at different stages of plant development. For instance, genes involved in streptomycin synthesis were significantly induced at bolting and flowering stages, presumably for disease suppression. We surmise that plants secrete blends of compounds and specific phytochemicals in the root exudates that are differentially produced at distinct stages of development to help orchestrate rhizosphere microbiome assemblage.

SUBMITTER: Chaparro JM

PROVIDER: S-EPMC3960538 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Rhizosphere microbiome assemblage is affected by plant development.

Chaparro Jacqueline M JM Badri Dayakar V DV Vivanco Jorge M JM

The ISME journal 20131107 4

There is a concerted understanding of the ability of root exudates to influence the structure of rhizosphere microbial communities. However, our knowledge of the connection between plant development, root exudation and microbiome assemblage is limited. Here, we analyzed the structure of the rhizospheric bacterial community associated with Arabidopsis at four time points corresponding to distinct stages of plant development: seedling, vegetative, bolting and flowering. Overall, there were no sign ...[more]

PMID: 24196324

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Project description:BackgroundPlants have evolved intimate interactions with soil microbes for a range of beneficial functions including nutrient acquisition, pathogen resistance and stress tolerance. Further understanding of this system is a promising way to advance sustainable agriculture by exploiting the versatile benefits offered by the plant microbiome. The rhizosphere is the interface between plant and soil, and functions as the first step of plant defense and root microbiome recruitment. It features a specialized microbial community, intensive microbe-plant and microbe-microbe interactions, and complex signal communication. To decipher the rhizosphere microbiome assembly of soybean (Glycine max), we comprehensively characterized the soybean rhizosphere microbial community using 16S rRNA gene sequencing and evaluated the structuring influence from both host genotype and soil source.ResultsComparison of the soybean rhizosphere to bulk soil revealed significantly different microbiome composition, microbe-microbe interactions and metabolic capacity. Soil type and soybean genotype cooperatively modulated microbiome assembly with soil type predominantly shaping rhizosphere microbiome assembly while host genotype slightly tuned this recruitment process. The undomesticated progenitor species, Glycine soja, had higher rhizosphere diversity in both soil types tested in comparison to the domesticated soybean genotypes. Rhizobium, Novosphingobium, Phenylobacterium, Streptomyces, Nocardioides, etc. were robustly enriched in soybean rhizosphere irrespective of the soil tested. Co-occurrence network analysis revealed dominant soil type effects and genotype specific preferences for key microbe-microbe interactions. Functional prediction results demonstrated converged metabolic capacity in the soybean rhizosphere between soil types and among genotypes, with pathways related to xenobiotic degradation, plant-microbe interactions and nutrient transport being greatly enriched in the rhizosphere.ConclusionThis comprehensive comparison of the soybean microbiome between soil types and genotypes expands our understanding of rhizosphere microbe assembly in general and provides foundational information for soybean as a legume crop for this assembly process. The cooperative modulating role of the soil type and host genotype emphasizes the importance of integrated consideration of soil condition and plant genetic variability for future development and application of synthetic microbiomes. Additionally, the detection of the tuning role by soybean genotype in rhizosphere microbiome assembly provides a promising way for future breeding programs to integrate host traits participating in beneficial microbiota assembly.

Project description:BackgroundThe rhizosphere microbiome, which is shaped by host genotypes, root exudates, and plant domestication, is crucial for sustaining agricultural plant growth. Despite its importance, how plant domestication builds up specific rhizosphere microbiomes and metabolic functions, as well as the importance of these affected rhizobiomes and relevant root exudates in maintaining plant growth, is not well understood. Here, we firstly investigated the rhizosphere bacterial and fungal communities of domestication and wild accessions of tetraploid wheat using amplicon sequencing (16S and ITS) after 9 years of domestication process at the main production sites in China. We then explored the ecological roles of root exudation in shaping rhizosphere microbiome functions by integrating metagenomics and metabolic genomics approaches. Furthermore, we established evident linkages between root morphology traits and keystone taxa based on microbial culture and plant inoculation experiments.ResultsOur results suggested that plant rhizosphere microbiomes were co-shaped by both host genotypes and domestication status. The wheat genomes contributed more variation in the microbial diversity and composition of rhizosphere bacterial communities than fungal communities, whereas plant domestication status exerted much stronger influences on the fungal communities. In terms of microbial interkingdom association networks, domestication destabilized microbial network and depleted the abundance of keystone fungal taxa. Moreover, we found that domestication shifted the rhizosphere microbiome from slow growing and fungi dominated to fast growing and bacteria dominated, thereby resulting in a shift from fungi-dominated membership with enrichment of carbon fixation genes to bacteria-dominated membership with enrichment of carbon degradation genes. Metagenomics analyses further indicated that wild cultivars of wheat possess higher microbial function diversity than domesticated cultivars. Notably, we found that wild cultivar is able to harness rhizosphere microorganism carrying N transformation (i.e., nitrification, denitrification) and P mineralization pathway, whereas rhizobiomes carrying inorganic N fixation, organic N ammonification, and inorganic P solubilization genes are recruited by the releasing of root exudates from domesticated wheat. More importantly, our metabolite-wide association study indicated that the contrasting functional roles of root exudates and the harnessed keystone microbial taxa with different nutrient acquisition strategies jointly determined the aboveground plant phenotypes. Furthermore, we observed that although domesticated and wild wheats recruited distinct microbial taxa and relevant functions, domestication-induced recruitment of keystone taxa led to a consistent growth regulation of root regardless of wheat domestication status.ConclusionsOur results indicate that plant domestication profoundly influences rhizosphere microbiome assembly and metabolic functions and provide evidence that host plants are able to harness a differentiated ecological role of root-associated keystone microbiomes through the release of root exudates to sustain belowground multi-nutrient cycles and plant growth. These findings provide valuable insights into the mechanisms underlying plant-microbiome interactions and how to harness the rhizosphere microbiome for crop improvement in sustainable agriculture. Video Abstract.

Project description:Bacterial communities associated with plant roots play an important role in the suppression of soil-borne pathogens, and multispecies probiotic consortia may enhance disease suppression efficacy. Here we introduced defined Pseudomonas species consortia into naturally complex microbial communities and measured the importance of Pseudomonas community diversity for their survival and the suppression of the bacterial plant pathogen Ralstonia solanacearum in the tomato rhizosphere microbiome. The survival of introduced Pseudomonas consortia increased with increasing diversity. Further, high Pseudomonas diversity reduced pathogen density in the rhizosphere and decreased the disease incidence due to both intensified resource competition and interference with the pathogen. These results provide novel mechanistic insights into elevated pathogen suppression by diverse probiotic consortia in naturally diverse plant rhizospheres. Ecologically based community assembly rules could thus play a key role in engineering functionally reliable microbiome applications.ImportanceThe increasing demand for food supply requires more-efficient control of plant diseases. The use of probiotics, i.e., naturally occurring bacterial antagonists and competitors that suppress pathogens, has recently reemerged as a promising alternative to agrochemical use. It is, however, still unclear how many and which strains we should choose for constructing effective probiotic consortia. Here we present a general ecological framework for assembling effective probiotic communities based on in vitro characterization of community functioning. Specifically, we show that increasing the diversity of probiotic consortia enhances community survival in the naturally diverse rhizosphere microbiome, leading to increased pathogen suppression via intensified resource competition and interference with the pathogen. We propose that these ecological guidelines can be put to the test in microbiome engineering more widely in the future.

Project description:The substrate pH directly affects nutrient availability in the rhizosphere and nutrient uptake by plants. Macronutrients such as nitrogen, potassium, calcium, magnesium, and sulfur are highly available at pH 6.0-6.5, while micronutrients become less available at higher, alkaline pH (pH > 7.0). Recent research has indicated that low pHs can enhance nutrient uptake and improve sweet orange (Citrus sinensis) tree health. We designed a study to understand the influence of a wide range of substrate pH values on plant size and biomass, nutrient availability, leaf gas exchange, and rhizosphere microbiome of grapefruit (Citrus paradisi) affected by Huanglongbing (HLB). Two-year-old "Ray Ruby" grapefruit plants grafted on sour orange (Citrus aurantium) rootstock were cultivated indoors in 10-cm wide × 40-cm tall pots with peat:perlite commercial substrate (80:20 v/v). We tested two disease statuses [HLB-free or healthy (negative, HLB-) and HLB-affected (positive, HLB+)] and six substrate pH values (4, 5, 6, 7, 8, 9) in a 2 × 6 factorial arranged on a complete randomized design with four replications. The canopy volume of HLB+ plants was 20% lower than healthy plants, with pHs 7 and 9 resulting in 44% less canopy volume. The root and shoot ratio of dry weight was 25.8% lower in HLB+ than in healthy plants. Poor root growth and a decrease in fibrous roots were found, especially in pH 5 and 6 treatments in HLB+ plants (p < 0.0001). The disease status and the substrate pHs influenced the leaf nutrient concentration (p < 0.05). High substrate pH affects nutrient availability for root uptake, influencing the nutrient balance throughout the plant system. pH values did not affect plant photosynthesis, indicating that pH does not recover HLB+ plants to the photosynthetic levels of healthy plants-even though high pH positively influenced internal CO2. There were collectively over 200 rhizobacterial identified by the 16S rRNA gene sequencing in individual phylogenetic trees. Most rhizobacteria reads were identified in pH 9. Our results indicated no effect of substrate pHs on the plant disease status induced by enhanced nutrient uptake.

Project description:The interactions between rhizosphere microorganisms and plants are important for the health and development of crops. Analysis of plant rhizosphere bacterial compositions, particularly of those with resistance to biotic/abiotic stresses, may improve their applications in sustainable agriculture. Large-scale rhizosphere samplings in the field are usually required; however, such samples, cannot be immediately frozen. We found that the storage of samples at room temperature for 2 days leads to a considerable reduction in the operational taxonomic unit (OTU) number and the indices of bacterial alpha-diversity of rhizosphere communities. In this study, in order to overcome these problems, we established a method using guanidine thiocyanate (GTC) solution for the preservation of rhizosphere samples after their collection. This method allowed the maintenance of the samples for at least 1 day at room temperature prior to their cryopreservation and was shown to be compatible with conventional DNA isolation protocols. Illumina sequencing of V3 and V4 hypervariable regions of the 16S rRNA gene was used to assess the feasibility and reliability of this method, and no significant differences were observed in the number of OTUs and in the Chao and Shannon indices between samples stored at -70 °C and those stored in GTC solution. Moreover, the representation of Pseudomonas spp. in samples stored in GTC solution was not significantly different from that in samples stored at -70 °C, as determined by real-time quantitative polymerase chain reaction (p > 0.05). Both types of samples were shown to cluster together according to principal coordinate analysis. Furthermore, GTC solution did not affect the bacterial taxon profiles at different storage periods compared with those observed when storing the samples below -70 °C. Even incubation of thawed samples (frozen at -70 °C) for 15 min at room temperature induced minor changes in the bacterial composition. Taken together, our results demonstrated that GTC solution may provide a reliable alternative for the preservation of rhizosphere samples in the field.

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Rhizosphere microbiome assemblage is affected by plant development.

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Rhizosphere microbiome assemblage is affected by plant development.

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