Symbiotic mutualisms provide critical ecosystem services throughout the world. Anthropogenic stressors, however, may disrupt mutualistic interactions and impact ecosystem health. The plant‐rhizobia symbiosis promotes plant growth and contributes to the nitrogen (N) cycle. While off‐target herbicide exposure is recognized as a significant stressor impacting wild plants, we lack knowledge about how it affects the symbiotic relationship between plants and rhizobia. Moreover, we do not know whether the impact of herbicide exposure on symbiotic traits or plant fitness might be ameliorated by plant or rhizobial genetic variation. To address these gaps, we conducted a greenhouse study where we grew 17 full‐sibling genetic families of red clover (Trifolium pratense) either alone (uninoculated) or in symbiosis with one of two genetic strains of rhizobia (Rhizobium leguminosarum) and exposed them to a concentration of the herbicide dicamba that simulated “drift” (i.e., off‐target atmospheric movement) or a control solution. We recorded responses in immediate vegetative injury, key features of the plant‐rhizobia mutualism (nodule number, nodule size, and N fixation), mutualism outcomes, and plant fitness (biomass). In general, we found that rhizobial variation more than plant variation determined outcomes of mutualism and plant fitness in response to herbicide exposure. Herbicide damage response depended on plant family, but also whether plants were inoculated with rhizobia and if so, with which strain. Rhizobial strain variation determined nodule number and size, but this was herbicide treatment‐dependent. In contrast, strain and herbicide treatment independently impacted symbiotic N fixation. And while herbicide exposure significantly reduced plant fitness, this effect depended on inoculation state. Furthermore, the differential fitness benefits that the two rhizobial strains provided plants seemed to diminish under herbicidal conditions. Altogether, these findings suggest that exposure to low levels of herbicide impact key components of the plant‐rhizobia mutualism as well as plant fitness, but genetic variation in the partners determines the magnitude and/or direction of these effects. In particular, our results highlight a strong role of rhizobial strain identity in driving both symbiotic and plant growth responses to herbicide stress.

中文翻译：

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根瘤菌变异比植物变异更能介导植物对除草剂胁迫的共生和适应性反应


共生共生在全世界提供关键的生态系统服务。然而，人为压力源可能会破坏互惠互利的互动并影响生态系统健康。植物-根瘤菌共生促进植物生长并有助于氮 （N） 循环。虽然脱靶除草剂暴露被认为是影响野生植物的重要压力源，但我们缺乏关于它如何影响植物和根瘤菌之间共生关系的知识。此外，我们不知道除草剂暴露对共生性状或植物适应性的影响是否可以通过植物或根瘤菌遗传变异来改善。为了解决这些差距，我们进行了一项温室研究，我们培养了 17 个红三叶草 （Trifolium pratense） 的全兄弟遗传家族，要么单独（未接种）或与两种根瘤菌遗传菌株之一 （Rhizobium leguminosarum） 共生，并将它们暴露于模拟“漂移”（即脱靶大气运动）或对照溶液的除草剂麦草畏浓度。我们记录了即时营养损伤、植物-根瘤菌共生的关键特征（根瘤数量、根瘤大小和 N 固定）、共生结果和植物适应性（生物量）的反应。一般来说，我们发现根瘤菌变异比植物变异更能决定响应除草剂暴露的共生关系和植物适应性的结果。除草剂损害反应取决于植物科，但也取决于植物是否接种了根瘤菌，如果接种，则接种了哪种菌株。根瘤菌株变异决定了根瘤的数量和大小，但这是依赖于除草剂处理的。相比之下，菌株和除草剂处理独立影响共生 N 固定。 虽然除草剂暴露会显著降低植物的适应性，但这种效果取决于接种状态。此外，在除草条件下，两种根瘤菌菌株为植物提供的差异适应性益处似乎减弱了。总而言之，这些发现表明，暴露于低水平除草剂会影响植物与根瘤菌共生的关键组成部分以及植物适应性，但伙伴的遗传变异决定了这些影响的大小和/或方向。特别是，我们的结果强调了根瘤菌菌株身份在驱动共生和植物生长对除草剂胁迫的反应中的重要作用。