Land plants associate with a root microbiota distinct from the complex microbial community present in surrounding soil. The microbiota colonizing therhizosphere(immediately surroundingthe root) and the endophytic compartment (within the root) contribute to plant growth, productivity, carbon sequestration and phytoremediation1-3. Colonization of the root occurs despite a sophisticated plant immune system4,5, suggesting finely tuned discrimination of mutualists and commensals from pathogens. Genetic principles governing the derivation of host-specific endophyte communities from soil communities are poorly understood. Here we report the pyrosequencing of the bacterial 16S ribosomal RNA gene of more than 600 Arabidopsis thaliana plants to test the hypotheses that the root rhizosphere and endophytic compartment microbiota of plants grown under controlled conditions in natural soils are sufficiently dependent on the host to remain consistent across different soil types and developmental stages, and sufficiently dependent on host genotype to vary between inbred Arabidopsis accessions. We describe different bacterial communities in two geochemically distinct bulk soils and in rhizosphere and endophytic compartments prepared from roots grown in these soils. The communities in each compartment are strongly influenced by soil type. Endophytic compartments from both soils feature overlapping, low-complexity communities that are markedly enriched in Actinobacteria and specific families from other phyla, notably Proteobacteria. Some bacteria vary quantitatively between plants of different developmental stage and genotype. Our rigorous definition of an endophytic compartment microbiome should facilitate controlled dissection of plantmicrobe interactions derived from complex soil communities.

Immune systems distinguish "self" from "nonself" to maintain homeostasis and must differentially gate access to allow colonization by potentially beneficial, nonpathogenic microbes. Plant roots grow within extremely diverse soil microbial communities but assemble a taxonomically limited root-associated microbiome. We grew isogenic Arabidopsis thaliana mutants with altered immune systems in a wild soil and also in recolonization experiments with a synthetic bacterial community. We established that biosynthesis of, and signaling dependent on, the foliar defense phytohormone salicylic acid is required to assemble a normal root microbiome. Salicylic acid modulates colonization of the root by specific bacterial families. Thus, plant immune signaling drives selection from the available microbial communities to sculpt the root microbiome.

Plants live in biogeochemically diverse soils that harbor extraordinarily diverse microbiota. Plant organs associate intimately with a subset of these microbes; this community’s structure can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients; they can also provide traits that increase plant productivity. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. We establish that a genetic network controlling phosphate stress response influences root microbiome community structure, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defense in the presence of a synthetic bacterial community. We demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis also directly repress defense, consistent with plant prioritization of nutritional stress over defense. Our work will impact efforts to define and deploy useful microbes to enhance plant performance.

Plants intimately associate with diverse bacteria. Plant-associated (PA) bacteria have ostensibly evolved genes enabling adaptation to the plant environment. However, the identities of such genes are mostly unknown and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3837 bacterial genomes to identify thousands of PA gene clusters. Genomes of PA bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant associated genomes. We experimentally validated candidates from two sets of PA genes, one involved in plant colonization, the other serving in microbe-microbe competition between PA bacteria. We also identified 64 PA protein domains that potentially mimic plant domains; some are shared with PA fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides leads for efficient and sustainable agriculture through microbiome engineering.

After a century of incremental research, technological advances, coupled with a need for sustainable crop yield increases, have reinvigorated the study of beneficial plant-microbe interactions with attention focused on how microbiomes alter plant phenotypes. We review recent advances in plant microbiome research, and describe potential applications for increasing crop productivity. The phylogenetic diversity of plant microbiomes is increasingly well characterized, and their functional diversity is becoming more accessible. Large culture collections are available for controlled experimentation, with more to come. Genetic resources are being brought to bear on questions of microbiome function. We expect that microbial amendments of varying complexities will expose rules governing beneficial plant-microbe interactions contributing to plant growth promotion and disease resistance, enabling more sustainable agriculture.

The second-generation antipsychotic olanzapine is effective in reducing psychotic symptoms but can cause extreme weight gain in human patients. We investigated the role of the gut microbiota in this adverse drug effect using a mouse model. First, we used germ-free C57BL/6J mice to demonstrate that gut bacteria are necessary and sufficient for weight gain caused by oral delivery of olanzapine. Second, we surveyed fecal microbiota before, during, and after treatment and found that olanzapine potentiated a shift towards an “obesogenic” bacterial profile. Finally, we demonstrated that olanzapine has antimicrobial activity in vitro against resident enteric bacterial strains. These results collectively provide strong evidence for a mechanism underlying olanzapine-induced weight gain in mouse and a hypothesis for clinical translation in human patients.

Specific members of complex microbiota can influence host phenotypes, depending on both the abiotic environment and the presence of other microorganisms. Therefore, it is challenging to define bacterial combinations that have predictable host phenotypic outputs. We demonstrate that plant–bacterium binary-association assays inform the design of small synthetic communities with predictable phenotypes in the host. Specifically, we constructed synthetic communities that modified phosphate accumulation in the shoot and induced phosphate starvation–responsive genes in a predictable fashion. We found that bacterial colonization of the plant is not a predictor of the plant phenotypes we analyzed. Finally, we demonstrated that characterizing a subset of all possible bacterial synthetic communities is sufficient to predict the outcome of untested bacterial consortia. Our results demonstrate that it is possible to infer causal relationships between microbiota membership and host phenotypes and to use these inferences to rationally design novel communities.

Summary1. The role of both plants and soil microbes on ecosystem functioning has been long recognized, but the precise feedback mechanisms between them are more elusive. Definition of these interactions is critical if we aim to achieve an integral understanding of ecosystem functioning, and ultimately explain natural, agricultural and synthetic systems. 2. Advances in genomic technologies and the development of more appropriate statistical, mathematical and computational frameworks enable researchers to almost fully describe and measure the diversity of microbial communities in soil, rhizosphere and plant tissues. Under the scaffold of community ecology, we integrate the observed patterns of microbial diversity with current mechanistic understanding of plant-microbe mutualistic and pathogenic interactions, and propose a model in which plant microbial communities are shaped by different ecological forces differentially through the plant life cycle. 3. The same genomic technologies, applied on natural and reconstructed systems, establish that plant genotype has a small, but significant, effect on the microbial community composition in, on and around plant organs. Despite these advances, technical limitations are still important and only a handful of studies exist where a precise genetic element definitively participates in these interactions. 4. Studies at the field or ecosystem level are dominated by agricultural settings, examining microbial species and communities effects on plant productivity; and conversely, that plant genetics and agricultural practices can potentially impose selective pressures on specific microbes and microbial communities. 5. Revitalized interest in plant-soil microbial feedbacks requires researchers to systematically pose and evaluate more complex hypotheses with increasingly more realistic microbial settings. Despite the advances reviewed here, most studies focus on one aspect of plant, microbe and soil interactions. Experiments that simultaneously and methodically manipulate multiple components are necessary to establish the ecological principles, and molecular mechanisms, which drive microbially mediated plant-soil interactions. This knowledge will be critical to predict how environmental changes affect microbial and plant diversity, and will guide efforts to improve agricultural and conservation practices.