Plants provide multitude of niches for the growth and proliferation of a diversity of microorganisms, including bacteria, fungi, protists, nematodes, and viruses (the plant microbiota). The microbiome (microbiota and their genomes) inhabiting the soil, rhizosphere, roots, and other plant tissues establishes complex and dynamic multitrophic interactions with the host plant. Deciphering the dialogues through which abiotic stresses such as drought reshape these multitrophic interactions is essential for developing strategies to increase plant resilience to climate stress. However, the chemical signals and molecular mechanisms by which the host stress responses influence the plant-microbiome are poorly studied. In a large greenhouse experiment, we tested the impact of soil factors, drought, and wheat genotype on plant fitness and the multitrophic interactions within the plant-associated microbiome. Our results showed that drought influences the relative importance, frequency, and composition of functional groups, their trophic interactions, and the processes controlling them. Furthermore, the co-existence network showed that drought significantly influences intra- and inter-kingdom microbial associations, increasing the hubs taxa belonging to protists. In addition, changes in the chemodiversity of the root exudates were linked to dynamic changes in the multitrophic interactions. We postulate that changes in the plant immune response and hormonal signaling in response to drought play a significant role in shaping composition and interactions between different members of plant-associated microbiome. A better mechanistic understanding of the multitrophic plant–microbiome interactions will be a step forward in developing future tools to predict and mitigate the impacts of climate change on primary productivity and plant diversity.
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