Soybean symbiosis isn't what it used to be
Older soybean varieties benefit more from mixtures of good and bad symbiotic nitrogen-fixing bacteria than modern soybean varieties do. This work has also been
discussed on the Nature website by Heidi Ledford and on the Agricultural Biodiversity Weblog by Jeremy Cherfas.
"variations... profitable to the individuals of a species... will tend to the preservation of such individuals, and will generally be inherited by the offspring. I have called this principle... natural selection, in order to mark its relation to man's power of selection."Darwin was rightly impressed by what plant breeders have accomplished. I'm glad that potato breeders have reduced poisonous tomatine concentrations enough that we no longer need to eat absorbent clay with our potatoes, as was necessary with wild potatoes (Johns, 1990 p. 92). But sometimes selecting for a beneficial trait can have negative side effects. This problem applies both to natural selection and to selection by humans. Trade-offs among desirable traits can result from physical linkage between genes, intrinsic constraints (a given amount of sugar can be diluted in a larger strawberry), or random drift in traits not under selection.
-- (Darwin, 1859)
This week, Toby Kiers, Mark Hutton, and I are reporting an apparent decrease, over the course of 60 years of soybean breeding, in the ability of plants to benefit from rhizobium bacteria. Our paper "Human selection and the relaxation of legume defences against ineffective rhizobia" is published on-line in Proceedings of the Royal Society.
Rhizobia are soil bacteria best known for infecting legume plants and proliferating inside root nodules, where they typically convert ("fix") atmospheric nitrogen into forms plants can use. Rhizobia in most soils vary in the benefits they provide. A survey of soybean rhizobia in the US found that "25% were highly effective, 50 percent only average, and the rest poor or ineffective" (Erdman, 1950). Soybeans tend to conserve photosynthate by sending more of it to whichever nodules are fixing the most nitrogen (Singleton and Stockinger, 1983). This allows rhizobia that fix more nitrogen to reproduce more inside nodules, relative to those that fix less (Kiers et al., 2003). Without these "host sanctions", rhizobia that allocate more resources to their own reproduction, at the expense of nitrogen fixation, would have displaced more beneficial rhizobium strains over the course of evolution (Denison, 2000; West et al., 2002).
Do plants vary in sanctions as much as rhizobia vary in nitrogen fixation? If so, have sanctions evolved differently in agricultural species subject to human selection, relative to wild species with only natural selection? Toby Kiers (my former PhD student, now at Vrije Universiteit Amsterdam) hypothesized that increased availability of nitrogen fertilizer since 1940 may have reduced the importance of nitrogen fixation as a selection criterion in plant breeding programs. (Nitrogen is not usually applied directly to nitrogen-fixing crops, but carryover from previous crops like corn can be significant.) Alternatively, the greater availability of soil nitrogen might raise the bar for rhizobia, allowing plants to shut down all but the best-performing nodules.
To test these hypotheses, we designed a field experiment, which she conducted in Maine with collaborator Mark Hutton. They used fields where soybeans had not been grown before, so she could expose plants to any combination of good and bad rhizobia. When the soil contained a 50:50 mix of fixing and nonfixing rhizobia, older varieties (3 bars at left) yielded at least as well as if only good rhizobia were present (dashed line in figure) but newer varieties did worse. As a result, the yield advantage of newer varieties disappeared with this mix of good and bad rhizobia (lower panel of figure). Although old varieties seemed to do better with the rhizobium mix than with good rhizobia alone, this apparent benefit was not statistically significant.
It seems unlikely that plant breeders and farmers would have failed to notice a lack of progress in soybean yields over decades, so maybe improvements in other genetic traits (better resistance to diseases not present in Maine, for example) have outweighed any deterioration in rhizobium interactions, for most farmers. It is also possible that the rhizobium mix used was worse than what is present in the soil of many commercial fields. Or there may be enough left-over nitrogen in many fields that nitrogen fixation is less critical. Given the high energy cost of nitrogen fertilizer and its contribution to water pollution, however, substituting fertilizer for nitrogen fixation is probably a bad idea.
Are host sanctions in the older varieties optimal? I suspect not. Although natural selection (or human selection based on yield in a low-nitrogen soil with a mixture of good and bad rhizobia) would presumably maintain sanctions against the very worst rhizobia, mediocre strains might be tolerated, if they provide more immediate benefit than immediate cost to the plant. But allowing mediocre strains to reproduce in nodules and escape into the soil means that the next soybean crop will also be plagued with mediocre rhizobia. A better longer-term approach would be to breed legume crops that impose sanctions severe enough to selectively enrich the soil with only the best rhizobium strains. Natural selection is blind to long-term considerations, but we need not be -- budget deficits, over-harvesting of forests and fish, and under-investment in research and education notwithstanding!
Darwin, C.R. 1859. The origin of species (reprinted 1962). Collier, New York.
Denison, R.F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156:567-576.
Erdman, L.W. 1950. Legume inoculation. USDA Farmer's Bull. 2003:1-20.
Johns, T. 1990. The origins of human diet and medicine. University of Arizona Press, Tuscon.
Kiers, E.T., R.A. Rousseau, S.A. West and R.F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.
Singleton, P.W. and K.R. Stockinger. 1983. Compensation against ineffective nodulation in soybean. Crop Sci. 23:69-72.
West, S.A., E.T. Kiers, E.L. Simms and R.F. Denison. 2002. Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proc. R. Soc. Lond. B 269:685-694.