Root microbiota drive direct integration of phosphate stress and immunity.
ABSTRACT: Plants live in biogeochemically diverse soils with diverse microbiota. Plant organs associate intimately with a subset of these microbes, and the structure of the microbial community can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients, but may also carry traits that increase the productivity of the plant. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. Here we establish that a genetic network controlling the phosphate stress response influences the structure of the root microbiome community, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defence in the presence of a synthetic bacterial community. We further demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis thaliana also directly repress defence, consistent with plant prioritization of nutritional stress over defence. Our work will further efforts to define and deploy useful microbes to enhance plant performance.
Project description:Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.
Project description:Plants growing in soil develop close associations with soil microorganisms, which inhabit the areas around, on, and inside their roots. These microbial communities and their associated genes - collectively termed the root microbiome - are diverse and have been shown to play an important role in conferring abiotic stress tolerance to their plant hosts. In light of growing concerns over the threat of water and nutrient stress facing terrestrial ecosystems, especially those used for agricultural production, increased emphasis has been placed on understanding how abiotic stress conditions influence the composition and functioning of the root microbiome and the ultimate consequences for plant health. However, the composition of the root microbiome under abiotic stress conditions will not only reflect shifts in the greater bulk soil microbial community from which plants recruit their root microbiome but also plant responses to abiotic stress, which include changes in root exudate profiles and morphology. Exploring the relative contributions of these direct and plant-mediated effects on the root microbiome has been the focus of many studies in recent years. Here, we review the impacts of abiotic stress affecting terrestrial ecosystems, specifically flooding, drought, and changes in nitrogen and phosphorus availability, on bulk soil microbial communities and plants that interact to ultimately shape the root microbiome. We conclude with a perspective outlining possible directions for future research needed to advance our understanding of the complex molecular and biochemical interactions between soil, plants, and microbes that ultimately determine the composition of the root microbiome under abiotic stress.
Project description:The microbiome of flowers (anthosphere) is an understudied compartment of the plant microbiome. Within the flower, petals represent a heterogeneous environment for microbes in terms of resources and environmental stress. Yet, little is known of drivers of structure and function of the epiphytic microbial community at the within-petal scale. We characterized the petal microbiome in two co-flowering plants that differ in the pattern of ultraviolet (UV) absorption along their petals. Bacterial communities were similar between plant hosts, with only rare phylogenetically distant species contributing to differences. The epiphyte community was highly culturable (75% of families) lending confidence in the spatially explicit isolation and characterization of bacteria. In one host, petals were heterogeneous in UV absorption along their length, and in these, there was a negative relationship between growth rate and position on the petal, as well as lower UV tolerance in strains isolated from the UV-absorbing base than from UV reflecting tip. A similar pattern was not seen in microbes isolated from a second host whose petals had uniform patterning along their length. Across strains, the variation in carbon usage and chemical tolerance followed common phylogenetic patterns. This work highlights the value of petals for spatially explicit explorations of bacteria of the anthosphere.
Project description:The soil-plant ecosystem harbors an immense microbial diversity that challenges investigative approaches to study traits underlying plant-microbe association. Studies solely based on culture-dependent techniques have overlooked most microbial diversity. Here we describe the concomitant use of culture-dependent and -independent techniques to target plant-beneficial microbial groups from the sugarcane microbiome. The community-based culture collection (CBC) approach was used to access microbes from roots and stalks. The CBC recovered 399 unique bacteria representing 15.9% of the rhizosphere core microbiome and 61.6-65.3% of the endophytic core microbiomes of stalks. By cross-referencing the CBC (culture-dependent) with the sugarcane microbiome profile (culture-independent), we designed a synthetic community comprised of naturally occurring highly abundant bacterial groups from roots and stalks, most of which has been poorly explored so far. We then used maize as a model to probe the abundance-based synthetic inoculant. We show that when inoculated in maize plants, members of the synthetic community efficiently colonize plant organs, displace the natural microbiota and dominate at 53.9% of the rhizosphere microbial abundance. As a result, inoculated plants increased biomass by 3.4-fold as compared to uninoculated plants. The results demonstrate that abundance-based synthetic inoculants can be successfully applied to recover beneficial plant microbes from plant microbiota.
Project description:Mechanisms used by plants to respond to water limitation have been extensively studied. However, even though the inoculation of beneficial microbes has been shown to improve plant performance under drought stress, the inherent role of soil microbes on plant response has been less considered. In the present work, we assessed the importance of the soil microbiome for the growth of barley plants under drought stress. Plant growth was not significantly affected by the disturbance of the soil microbiome under regular watering. However, after drought stress, we observed a significant reduction in plant biomass, particularly of the root system. Plants grown in the soil with disturbed microbiome were significantly more affected by drought and did not recover two weeks after re-watering. These effects were accompanied by changes in the composition of endophytic fungal and bacterial communities. Under natural conditions, soil-derived plant endophytes were major colonizers of plant roots, such as Glycomyces and Fusarium, whereas, for plants grown in the soil with disturbed microbiome seed-born bacterial endophytes, e.g., Pantoea, Erwinia, and unclassified Pseudomonaceae and fungal genera normally associated with pathogenesis, such as Gibberella and Gaeumannomyces were observed. Therefore, the role of the composition of the indigenous soil microbiota should be considered in future approaches to develop management strategies to make plants more resistant towards abiotic stress, such as drought.
Project description:Plant-associated microbes are important for the growth and health of their hosts. As a result of numerous prior studies, we know that host genotypes and abiotic factors influence the composition of plant microbiomes. However, the high complexity of these communities challenges detailed studies to define experimentally the mechanisms underlying the dynamics of community assembly and the beneficial effects of such microbiomes on plant hosts. In this work, from the distinctive microbiota assembled by maize roots, through host-mediated selection, we obtained a greatly simplified synthetic bacterial community consisting of seven strains (Enterobacter cloacae, Stenotrophomonas maltophilia, Ochrobactrum pituitosum, Herbaspirillum frisingense, Pseudomonas putida, Curtobacterium pusillum, and Chryseobacterium indologenes) representing three of the four most dominant phyla found in maize roots. By using a selective culture-dependent method to track the abundance of each strain, we investigated the role that each plays in community assembly on roots of axenic maize seedlings. Only the removal of E. cloacae led to the complete loss of the community, and C. pusillum took over. This result suggests that E. cloacae plays the role of keystone species in this model ecosystem. In planta and in vitro, this model community inhibited the phytopathogenic fungus Fusarium verticillioides, indicating a clear benefit to the host. Thus, combined with the selective culture-dependent quantification method, our synthetic seven-species community representing the root microbiome has the potential to serve as a useful system to explore how bacterial interspecies interactions affect root microbiome assembly and to dissect the beneficial effects of the root microbiota on hosts under laboratory conditions in the future.
Project description:Root-rot disease caused by Fusarium oxysporum is a growing problem in agriculture for commercial cultivation of Panax notoginseng. Diverse microbes colonize plant roots, and numerous earlier studies have characterized the rhizospheric microbiome of P. notoginseng; nevertheless, the function of probiotic consortia on the rhizospheric microbiome against the root-rot disease remain elusive. We have compared and described the rhizospheric microbiome of lightly and severely diseased P. notoginseng as well as the interactions of the probiotic consortia and rhizospheric microbiome, and their function to alleviate the plant diseases were explored by inoculating probiotic consortia in bulk soil. From the perspective of microbial diversity, the rhizospheric dominant bacterial and fungal genera were utterly different between lightly and severely diseased plants. Through inoculating assembled probiotic consortia to diseased plant roots, we found that the application of probiotic consortia reshaped the rhizosphere microbiome, increasing the relative abundance of bacteria and fungi, while the relative abundance of potential pathogens was decreased significantly. We developed a microcosm system that provides a preliminary ecological framework for constructing an active probiotic community to reshape soil microbiota and restrain the disease. Microbial community structure differs between lightly and seriously diseased plants. The application of probiotic consortia changes the imbalance of micro-ecology to a state of relative health, reducing plant mortality. Plant disease suppression may be achieved by seeking and applying antagonistic microbes based on their direct inhibitory capability or by restructuring the soil microbiome structure and function.
Project description:Some microbes enhance stress tolerance in plants by minimizing plant ethylene levels via degradation of its immediate precursor, 1-aminocyclopropane-1-carboxylate (ACC), in the rhizosphere. In return, ACC is used by these microbes as a source of nitrogen. This mutualistic relationship between plants and microbes may be used to promote soil properties in stressful environments. In this study, we tested the hypothesis that amendments of ACC in soils reshape the structure of soil microbiome and alleviate the negative impacts of salinity on soil properties. We treated non-saline and artificially-developed saline soils with ACC in different concentrations for 14 days. The structure of soil microbiome, soil microbial properties and productivity were examined. Our results revealed that microbial composition of bacteria, archaea and fungi in saline soils was affected by ACC amendments; whereas community composition in non-saline soils was not affected. The amendments of ACC could not fully counteract the negative effects of salinity on soil microbial activities and productivity, but increased the abundance of ACC deaminase-encoding gene (acdS), enhanced soil microbial respiration, enzymatic activity, nitrogen and carbon cycling potentials and Arabidopsis biomass in saline soils. Collectively, our study indicates that ACC amendments in soils could efficiently ameliorate salinity impacts on soil properties and plant biomass production.
Project description:Soil microbes that colonize plant roots and are responsive to differences in plant genotype remain to be ascertained for agronomically important crops. From a very large-scale longitudinal field study of 27 maize inbred lines planted in three fields, with partial replication 5 y later, we identify root-associated microbiota exhibiting reproducible associations with plant genotype. Analysis of 4,866 samples identified 143 operational taxonomic units (OTUs) whose variation in relative abundances across the samples was significantly regulated by plant genotype, and included five of seven core OTUs present in all samples. Plant genetic effects were significant amid the large effects of plant age on the rhizosphere microbiome, regardless of the specific community of each field, and despite microbiome responses to climate events. Seasonal patterns showed that the plant root microbiome is locally seeded, changes with plant growth, and responds to weather events. However, against this background of variation, specific taxa responded to differences in host genotype. If shown to have beneficial functions, microbes may be considered candidate traits for selective breeding.
Project description:Adverse growth conditions can lead to decreased plant growth, productivity, and survival, resulting in poor yields or failure of crops and biofeedstocks. In some cases, the microbial community associated with plants has been shown to alleviate plant stress and increase plant growth under suboptimal growing conditions. A systematic understanding of how the microbial community changes under these conditions is required to understand the contribution of the microbiome to water utilization, nutrient uptake, and ultimately yield. Using a microbiome inoculation strategy, we studied how the belowground microbiome of Populus deltoides changes in response to diverse environmental conditions, including water limitation, light limitation (shading), and metal toxicity. While plant responses to treatments in terms of growth, photosynthesis, gene expression and metabolite profiles were varied, we identified a core set of bacterial genera that change in abundance in response to host stress. The results of this study indicate substantial structure in the plant microbiome community and identify potential drivers of the phytobiome response to stress. IMPORTANCE The identification of a common "stress microbiome" indicates tightly controlled relationships between the plant host and bacterial associates and a conserved structure in bacterial communities associated with poplar trees under different growth conditions. The ability of the microbiome to buffer the plant from extreme environmental conditions coupled with the conserved stress microbiome observed in this study suggests an opportunity for future efforts aimed at predictably modulating the microbiome to optimize plant growth.