Abstract
Agriculture has intensified the presence of chemical stressors in the rhizosphere-the region surrounding roots where critical plant-microbe interactions occur, such as those between leguminous plants and nitrogen-fixing rhizobial bacteria. Particularly, rhizospheric pesticide exposure can disrupt the efficacy of the plant-rhizobia mutualism and reduce plant productivity. However, it is unknown whether genetic variation in plants (G(P)), rhizobia (G(R)), or interactions between them and the pesticide environment (E), i.e., G(P or R) [Formula: see text] E, or G(P) [Formula: see text] G(R) [Formula: see text] E, could mitigate these negative outcomes. We grew two genotypes of the leguminous plant Trifolium pratense in symbiosis with each of eight genetic strains of its rhizobial partner Rhizobium spp. symbiovar trifolii. We exposed symbionts to the contemporary synthetic auxin herbicide dicamba or a control in the rhizosphere, and evaluated the symbiotic interaction and plant growth. Our results provide new evidence that rhizobial genetic variation drives herbicide impacts on mutualism outcomes through G(R) [Formula: see text] E interactions. Rhizospheric herbicide delayed rhizobial colonization of plants via root nodule formation, but its effects on the number of nodules and fixed nitrogen produced varied depending on rhizobial strain. Similarly, while herbicide exposure reduced plant size on average, the degree of this effect was mediated by rhizobial partner, suggesting that rhizobia could potentially function as an "extended genotype" for defense against herbicide damage. As the use of herbicides, particularly synthetic auxins, continues to escalate, our findings have important implications for how certain rhizobia could be selected to improve plant fitness in the face of these anthropogenically-released chemicals.