An evolutionary perspective on increasing net benefits to crops from symbiotic microbes

Plant-imposed, fitness-reducing sanctions against less-beneficial symbionts have been documented for rhizobia, mycorrhizal fungi, and fig wasps. Although most of our examples are for rhizobia, we argue that the evolutionary persistence of mutualism in any symbiosis would require such sanctions, if there are multiple symbiont genotypes per host plant. We therefore discuss methods that could be used to develop and assess crops with stricter sanctions. These include methods to screen strains for greater mutualism as resources to identify crop genotypes that impose stronger selection for mutualism. Single-strain experiments that measure costs as well as benefits have shown that diversion of resources by rhizobia can reduce nitrogen-fixation efficiency (N per C) and that some legumes can increase this efficiency by manipulating their symbionts. Plants in the field always host multiple strains with possible synergistic interactions, so benefits from different strains might best be compared by regressing plant growth or yield on each strain's abundance in a mixture. However, results from this approach have not yet been published. To measure legacy effects of stronger sanctions on future crops, single-genotype test crops could be planted in a field that recently had replicated plots with different genotypes of the sanction-imposing crop. Enhancing agricultural benefits from symbiosis may require accepting tradeoffs that constrained past natural selection, including tradeoffs between current and future benefits.