Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion.
ABSTRACT: 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:Terrestrial plants host phylogenetically and functionally diverse groups of below-ground microbes, whose community structure controls plant growth/survival in both natural and agricultural ecosystems. Therefore, understanding the processes by which whole root-associated microbiomes are organized is one of the major challenges in ecology and plant science. We here report that diverse root-associated fungi can form highly compartmentalized networks of coexistence within host roots and that the structure of the fungal symbiont communities can be partitioned into semi-discrete types even within a single host plant population. Illumina sequencing of root-associated fungi in a monodominant south beech forest revealed that the network representing symbiont-symbiont co-occurrence patterns was compartmentalized into clear modules, which consisted of diverse functional groups of mycorrhizal and endophytic fungi. Consequently, terminal roots of the plant were colonized by either of the two largest fungal species sets (represented by Oidiodendron or Cenococcum). Thus, species-rich root microbiomes can have alternative community structures, as recently shown in the relationships between human gut microbiome type (i.e., 'enterotype') and host individual health. This study also shows an analytical framework for pinpointing network hubs in symbiont-symbiont networks, leading to the working hypothesis that a small number of microbial species organize the overall root-microbiome dynamics.
Project description:Phytoremediation is a promising in situ green technology based on the use of plants to cleanup soils from organic and inorganic pollutants. Microbes, particularly bacteria and fungi, that closely interact with plant roots play key roles in phytoremediation processes. In polluted soils, the root-associated microbes contribute to alleviation of plant stress, improve nutrient uptake and may either degrade or sequester a large range of soil pollutants. Therefore, improving the efficiency of phytoremediation requires a thorough knowledge of the microbial diversity living in the rhizosphere and in close association with plant roots in both the surface and the endosphere. This study aims to assess fungal ITS and bacterial 16S rRNA gene diversity using high-throughput sequencing in rhizospheric soils and roots of three plant species (Solidago canadensis, Populus balsamifera, and Lycopus europaeus) growing spontaneously in three petroleum hydrocarbon polluted sedimentation basins. Microbial community structures of rhizospheric soils and roots were compared with those of microbes associated with arbuscular mycorrhizal fungal (AMF) spores to determine the links between the root and rhizosphere communities and those associated with AMF. Our results showed a difference in OTU richness and community structure composition between soils and roots for both bacteria and fungi. We found that petroleum hydrocarbon pollutant (PHP) concentrations have a significant effect on fungal and bacterial community structures in both soils and roots, whereas plant species identity showed a significant effect only on the roots for bacteria and fungi. Our results also showed that the community composition of bacteria and fungi in soil and roots varied from those associated with AMF spores harvested from the same plants. This let us to speculate that in petroleum hydrocarbon contaminated soils, AMF may release chemical compounds by which they recruit beneficial microbes to tolerate or degrade the PHPs present in the soil.
Project description:The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.
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: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:Plant roots harbor a large diversity of microorganisms that have an essential role in ecosystem functioning. To better understand the level of intimacy of root-inhabiting microbes such as arbuscular mycorrhizal fungi and bacteria, we provided (13)CO(2) to plants at atmospheric concentration during a 5-h pulse. We expected microbes dependent on a carbon flux from their host plant to become rapidly labeled. We showed that a wide variety of microbes occurred in roots, mostly previously unknown. Strikingly, the greatest part of this unsuspected diversity corresponded to active primary consumers. We found 17 bacterial phylotypes co-occurring within roots of a single plant, including five potentially new phylotypes. Fourteen phylotypes were heavily labeled with the (13)C. Eight were phylogenetically close to Burkholderiales, which encompass known symbionts; the others were potentially new bacterial root symbionts. By analyzing unlabeled and (13)C-enriched RNAs, we demonstrated differential activity in C consumption among these root-inhabiting microbes. Arbuscular mycorrhizal fungal RNAs were heavily labeled, confirming the high carbon flux from the plant to the fungal compartment, but some of the fungi present appeared to be much more active than others. The results presented here reveal the possibility of uncharacterized root symbioses.
Project description:The presence and composition of soil microbial communities has been shown to have a large impact on plant-plant interactions and consequently plant diversity and composition. The goal of the present study was to evaluate impact of arbuscular mycorrhizal fungi (AMF) and nitrogen-fixing bacteria, which constitutes an essential link between the soil and the plant's roots. A greenhouse pot experiment was conducted to evaluate the feasibility of using selected microbes to improve Hieracium pilosella and Medicago sativa growth on Zn-Pb-rich site. Results of studies revealed that biomass, the dry mass of shoots and roots, increased significantly when plants were inoculated with mycorrhizal fungi and nitrogen-fixing bacteria. The addition of Azospirillum sp. and Nostoc edaphicum without mycorrhiza suppressed plant growth. Single bacterial inoculation alone does not have a positive effect on M. sativa growth, while co-inoculation with AMF improved plant growth. Plant vitality (expressed by the performance index) was improved by the addition of microbes. However, our results indicated that even dry heat sterilization of the substratum created imbalanced relationships between soil-plant and plants and associated microorganisms. The studies indicated that AMF and N2-fixers can improve revegetation of heavy metal-rich industrial sites, if the selection of interacting symbionts is properly conducted.
Project description:Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host-microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere Streptomyces are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors.
Project description:The microbial community in the plant rhizosphere is vital to plant productivity and disease resistance. Alterations in the composition and diversity of species within this community could be detrimental if microbes suppressing the activity of pathogens are removed. Species of the insect-pathogenic fungus, Metarhizium, commonly employed as biological control agents against crop pests, have recently been identified as plant root colonizers and provide a variety of benefits (e.g. growth promotion, drought resistance, nitrogen acquisition). However, the impact of Metarhizium amendment on the rhizosphere microbiome has yet to be elucidated. Using Illumina sequencing, we examined the community profiles (bacteria and fungi) of common bean (Phaseolus vulgaris) rhizosphere (loose soil and plant root) after amendment with M. robertsii conidia, in the presence and absence of an insect host. Although alpha diversity was not significantly affected overall, there were numerous examples of plant growth-promoting organisms that significantly increased with Metarhizium amendment (Bradyrhizobium, Flavobacterium, Chaetomium, Trichoderma). Specifically, the abundance of Bradyrhizobium, a group of nitrogen-fixing bacteria, was confirmed to be increased using a qPCR assay with genus-specific primers. In addition, the ability of the microbiome to suppress the activity of a known bean root pathogen was assessed. The development of disease symptoms after application with Fusarium solani f. sp. phaseoli was visible in the hypocotyl and upper root of plants grown in sterilized soil but was suppressed during growth in microbiome soil and soil treated with M. robertsii. Successful amendment of agricultural soils with biocontrol agents such as Metarhizium necessitates a comprehensive understanding of the effects on the diversity of the rhizosphere microbiome. Such research is fundamentally important towards sustainable agricultural practices to improve overall plant health and productivity.
Project description:Highly diverse microbial assemblages colonize plant roots. It is still poorly understood whether different members of this root microbiome act synergistically by supplying different services (for example, different limiting nutrients) to plants and plant communities. In order to test this, we manipulated the presence of two widespread plant root symbionts, arbuscular mycorrhizal fungi and nitrogen-fixing rhizobia bacteria in model grassland communities established in axenic microcosms. Here, we demonstrate that both symbionts complement each other resulting in increased plant diversity, enhanced seedling recruitment and improved nutrient acquisition compared with a single symbiont situation. Legume seedlings obtained up to 15-fold higher productivity if they formed an association with both symbionts, opposed to productivity they reached with only one symbiont. Our results reveal the importance of functional diversity of symbionts and demonstrate that different members of the root microbiome can complement each other in acquiring different limiting nutrients and in driving important ecosystem functions.