A Darwinian perspective on improving nitrogen-fixation efficiency of legume crops and forages

Symbiotic nitrogen fixation by rhizobia in root nodules of crop and forage legumes provides substantial economic and environmental benefits. Nitrogen fixation could be increased in various ways, but most of these would cause a proportional increase in photosynthate costs. This might decrease rather than increase yields, as indicated by the poor performance of crops that make extra nodules. A hypothesis explaining such failures is that past natural selection is unlikely to have missed improvements to nitrogen fixation that are both simple (i.e. arising frequently through mutation) and free of fitness-reducing trade-offs. Various plant and rhizobial mutants that indiscriminately increase resource allocation to nitrogen fixation have presumably arisen frequently, but died out because fitness costs exceeded fitness benefits. Increasing nitrogen-fixation efficiency (gN/gC) may be possible, however, via more complex genetic changes or by accepting trade-offs rejected by natural selection. Two rhizobia strains had greater efficiency in legumes that caused swelling of rhizobial bacteroids in their nodules relative to the same strains in hosts that did not cause swelling. Increasing nodule occupancy by more efficient rhizobial strains could provide major benefits, once we recognize that less efficient strains may evolve or acquire competitive traits of more efficient strains without their greater efficiency. Some legume crops and forages reduce the relative reproduction of less beneficial rhizobia in their nodules. These 'host sanctions' are based on actual nitrogen fixation, not easily mimicked recognition signals. Further enhancing host sanctions could lead to legumes that selectively enrich soils with only the most beneficial local rhizobia.