A single dehydrogenase associated with symbiotic carbon polymer synthesis pathway drives ineffective partner quality between Medicago sativa and Sinorhizobium meliloti

Plants require quality microbial partners to for optimal symbiotic relationships. In the rhizobium-legume mutualism where symbiotic nitrogen fixation represents a critical aspect of the biogeochemical cycle and a pillar of sustainable agriculture, partner quality of rhizobium symbionts for legumes varies dramatically. Yet, little is understood about the genetics that underly variations in partner quality in rhizobia. We used a large scale genomics approach to hone in on specific genes associated with a dramatic difference in partner quality of displayed be on strain of Sinorhizobium meliloti. This strain, HM006, shows a highly efficient symbiotic relationship with the model legume Medicago truncatula, whereas the symbiosis with the alternate host Medicago sativa (the crop plant alfalfa) is highly limited relative to other strains. We determined that the inefficient partner quality with Medicago sativa is caused by a set of genes associated with symbiotic carbon polymer synthesis, a phenomenon that has long been associated with “cheating” in the rhizobium-legume symbiosis. However, our data indicates the limited partner quality is not explained by diversion of resources, but rather a single biochemical reaction that converts succinic semialdehyde to gamma-hydroxybutyrate during polymer synthesis. These data suggest that breakdowns in the mutualism may result from biochemical incompatibilities between symbiont and host metabolisms when the plant host of a given symbiont is varied.