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ABSTRACT Successful plant growth requires plants to minimize harm from antagonists and maximize benefit from mutualists. However, these outcomes may be difficult to achieve simultaneously, since plant defenses activated in response to antagonists can compromise mutualism function, and plant resources allocated to defense may trade off with resources allocated to managing mutualists. Here, we investigate how antagonist attack affects plant ability to manage mutualists with sanctions, in which a plant rewards cooperative mutualists and/or punishes uncooperative mutualists. We studied interactions among wild and domesticated pea plants, pea aphids, an aphid‐vectored virus (Pea Enation Mosaic Virus, PEMV), and mutualistic rhizobial bacteria that fix nitrogen in root nodules. Using isogenic rhizobial strains that differ in their ability to fix nitrogen and express contrasting fluorescent proteins, we found that peas demonstrated sanctions in both singly‐infected nodules and mixed‐infection nodules containing both strains. However, the plant's ability to manage mutualists in mixed‐infection nodules traded off with its ability to defend against antagonists: when plants were attacked by aphids, they stopped sanctioning within mixed‐infection nodules, and plants that exerted stricter sanctions within nodules during aphid attack accumulated higher levels of the aphid‐vectored virus, PEMV. Our findings suggest that plants engaged in defense against antagonists suffer a reduced ability to select for the most beneficial symbionts in mixed‐infection tissues. Mixed‐infection tissues may be relatively common in this mutualism, and reduced plant sanctions in these tissues could provide a refuge for uncooperative mutualists and compromise the benefit that plants obtain from mutualistic symbionts during antagonist attack. Understanding the conflicting selective pressures plants face in complex biotic environments will be crucial for breeding crop varieties that can maximize benefits from mutualists even when they encounter antagonists. 

Legumes are ecologically and economically important plants that contribute to nutrient cycling and agricultural sustainability, features tied to their intimate symbiosis with nitrogen-fixing rhizobia. However, rhizobia vary dramatically in quality, ranging from highly growth- promoting to nonbeneficial. Therefore, optimizing plant benefits from this symbiosis requires host mechanisms that select for beneficial rhizobia and limit losses to nonbeneficial strains. Here, we examine the considerable scientific progress made in decoding host control over rhizobia, empirically demonstrating both molecular and cellular mechanisms and their effects on symbiotic benefits. Pre-infection control requires plant production and detection of precise molecular signals to attract and select compatible rhizobia strains. Post-infection mechanisms leverage nodule- and cell-level compartmentalization of symbionts to enable host control over rhizobia development and proliferation in planta. These layers of host preferential allocation act as a series of sieves, each of which contributes to legume fitness by directing host resources to a narrowing subset of more-beneficial rhizobia. 

Abstract The rhizosphere has been called “one of the most complex ecosystems on earth” because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed aplant‐centric perspective when trying to harness the potential of microbiome‐derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, amicrobe‐centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context‐dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production.