Agriculture and the Disruption of Plant–Microbial Symbiosis

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. 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. 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. a scenario in which an allele affects more than one trait, at least one of which improves fitness and at least one of which is deleterious. host-associated microbes that generate a fitness benefit for hosts relative to hosts lacking the association. Such benefits can be context dependent: a microbe may only increase fitness under conditions where the benefits of microbial resources outweigh costs to the host. an evolutionary or ecological decrease in the magnitude of the interaction of plants with beneficial soil microbiota. Reduction of a symbiosis trait could have a deleterious, adaptive, or neutral impact on plant fitness. expanding populations experience stochastic loss of genetic diversity at their expansion front, thus increasing drift and adding to the burden of deleterious mutations in the population. fluctuations in allele frequencies driven by selection on variation at linked loci (i.e., genetic hitchhiking). random changes in allele frequencies within a population, usually owing to the chance disappearance of alleles. crossing of distinct breeding pools allowing for complementation of negative and/or positive features of parental types. genetic exchange that occurs between different species resulting from hybridization, followed by backcrossing of hybrids with one or both parent species. nonrandom association of alleles from independent loci in a population, usually arising from the inheritance of neighboring alleles that are not separated by recombination. natural selection that favors an allele, causing that allele to increase in frequency in a population. natural selection that disfavors a deleterious allele, causing that allele to be purged from a population. a parameter that estimates the relative role of purifying selection versus positive selection acting on a set of homologous protein-coding loci. Synonymous substitutions (ds) are changes in coding DNA sequences that do not lead to an altered amino acid, and are assumed to be neutral. Conversely, nonsynonymous substitutions (dN) alter amino acids, and can either be deleterious, neutral, or beneficial, depending on the function of the gene and how the genes expression interacts with the environment. breaking up of linkage between neighboring loci that occurs during meiosis. The reshuffling of alleles that occurs during recombination causes offspring to bear a unique combination of loci relative to parents. a constraint whereby a limited resource must be distributed between competing traits, such as growth versus reproduction. inherited traits that underlie host responses to beneficial microbes and/or regulate colonization and infection by beneficial microbes. Symbiosis traits encompass a variety of host phenotypes and mechanisms, including tissues that house microbes, signaling molecules that control infection, morphological or chemical traits that alter host benefit from microbes, and physiological and developmental systems that regulate microbial proliferation and transmission.