Legume sanctions and the evolution of symbiotic cooperation by rhizobia

The legume-rhizobium symbiosis is an ideal model for studying the factors that limit the evolution of microbial mutualists into parasites. Legumes are unable to consistently recognize parasitic rhizobia that, once established inside plant cells, use plant resources for their own reproduction rather than for N-2 fixation. Evolution of parasitism in rhizobia, driven partly by competition among multiple rhizobial strains infecting the same plant, may be countered by postinfection legume sanctions. Both the biochemical options for rhizobial cheating and the evolutionary effect of legume sanctions depend on differences in rhizobial life history associated with nodule type. In legumes with determinate nodule growth, rhizobia typically retain the ability to reproduce after differentiating into N-2-fixing bacteroids. Sanctions against individual bacteroids (e.g., acid hydrolases) would therefore select for cooperative rhizobia. In nodules with indeterminate growth, bacteroids generally lose the ability to reproduce, so legume sanctions against bacteroids would have no effect on rhizobial evolution. Whole-nodule sanctions (e.g., decreased nodule O-2 permeability) could be effective, via kin selection of undifferentiated rhizobia that persist in indeterminate nodules and replenish soil populations after nodule senescence. Mixed nodules could reduce the effectiveness of whole-nodule sanctions. The frequency of mixed nodules under field conditions is unknown.