Agriculture and the Disruption of Plant–Microbial Symbiosis

Domestication has transformed hundreds of wild plant species into productive cultivars for human utility. However, cultivation practices and intense artificial selection for yield may entail a hidden cost: the disruption of interactions between plants and beneficial microbiota. Here, we synthesize theory predicting that evolutionary trade-offs, genetic costs, and relaxed selection disrupt plant–microbial symbiosis under domestication, and review the wealth of new data interrogating these predictions in crops. We describe the agronomic practices, ecological scenarios, and genomic attributes that can result in the disruption of symbiosis, and highlight new work probing its molecular basis. To improve agricultural output and sustainability, research should develop breeding methods to optimize symbiotic outcomes in crop species. Many crops interact differently with beneficial microbiota compared with their wild relatives.Plant traits that regulate symbiosis can be disrupted because: (i) disruption of the trait is favored directly or indirectly by artificial selection; (ii) plant traits accumulate deleterious genetic mutations due to the demographics of the breeding population; or (iii) disruption of the trait is selectively neutral under agricultural conditions.These mechanisms generate distinct patterns of symbiosis trait evolution, each of which can be detected with trait-based and population-genetic analysis.Identifying mechanisms that result in symbiosis trait disruption in crops will be essential for future efforts to maximize the benefits of microbial symbiosis for crops.