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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. 

In mutualism, hosts select symbionts via partner choice and preferentially direct more resources to symbionts that provide greater benefits via sanctions. At the initiation of symbiosis, prior to resource exchange, it is not known how the presence of multiple symbiont options (i.e. the symbiont social environment) impacts partner choice outcomes. Furthermore, little research addresses whether hosts primarily discriminate among symbionts via sanctions, partner choice or a combination. We inoculated the legume , Acmispon wrangelianus, with 28 pairs of fluorescently labelled Mesorhizobium strains that vary continuously in quality as nitrogen-fixing symbionts. We find that hosts exert robust partner choice, which enhances their fitness. This partner choice is conditional such that a strain's success in initiating nodules is impacted by other strains in the social environment. This social genetic effect is as important as a strain's own genotype in determining nodulation and has both transitive (consistent) and intransitive (idiosyncratic) effects on the probability that a symbiont will form a nodule. Furthermore, both absolute and conditional partner choice act in concert with sanctions, among and within nodules. Thus, multiple forms of host discrimination act as a series of sieves that optimize host benefits and select for costly symbiont cooperation in mixed symbiont populations.