SignificanceDrought remains a critical obstacle to meeting the food demands of the coming century. Understanding the interplay between drought stress, plant development, and the plant microbiome is central to meeting this challenge. Here, we demonstrate that drought causes enrichment of a distinct set of microbes in roots, composed almost entirely of monoderms, which lack outer membranes and have thick cell walls. We demonstrate that under drought, roots increase the production of many metabolites, and that monoderms inhabiting the drought-treated rhizosphere exhibit increased activity of transporters connected with some of these same compounds. The discovery of this drought-induced enrichment and associated shifts in metabolite exchange between plant and microbe reveal a potential blueprint for manipulating plant microbiomes for improved crop fitness.

Drought is the most important environmental stress limiting crop yields. The C4 cereal sorghum [Sorghum bicolor(L.) Moench] is a critical food, forage, and emerging bioenergy crop that is notably drought-tolerant. We conducted a large-scale field experiment, imposing preflowering and postflowering drought stress on 2 genotypes of sorghum across a tightly resolved time series, from plant emergence to postanthesis, resulting in a dataset of nearly 400 transcriptomes. We observed a fast and global transcriptomic response in leaf and root tissues with clear temporal patterns, including modulation of well-known drought pathways. We also identified genotypic differences in core photosynthesis and reactive oxygen species scavenging pathways, highlighting possible mechanisms of drought tolerance and of the delayed senescence, characteristic of the stay-green phenotype. Finally, we discovered a large-scale depletion in the expression of genes critical to arbuscular mycorrhizal (AM) symbiosis, with a corresponding drop in AM fungal mass in the plants’ roots.

Recent studies have demonstrated that drought leads to dramatic, highly conserved shifts in the root microbiome. At present, the molecular mechanisms underlying these responses remain largely uncharacterized. Here we employ genome-resolved metagenomics and comparative genomics to demonstrate that carbohydrate and secondary metabolite transport functionalities are overrepresented within drought-enriched taxa. These data also reveal that bacterial iron transport and metabolism functionality is highly correlated with drought enrichment. Using time-series root RNA-Seq data, we demonstrate that iron homeostasis within the root is impacted by drought stress, and that loss of a plant phytosiderophore iron transporter impacts microbial community composition, leading to significant increases in the drought-enriched lineage, Actinobacteria. Finally, we show that exogenous application of iron disrupts the drought-induced enrichment of Actinobacteria, as well as their improvement in host phenotype during drought stress. Collectively, our findings implicate iron metabolism in the root microbiome’s response to drought and may inform efforts to improve plant drought tolerance to increase food security.