Modern agriculture intensely selects aboveground plant structures, while often neglecting belowground features, and evolutionary tradeoffs between these traits are predicted to disrupt host control over microbiota. Moreover, drift, inbreeding, and relaxed selection for symbiosis in crops might degrade plant mechanisms that support beneficial microbes. We studied the impact of domestication on the nitrogen-fixing symbiosis between cowpea and root-nodulating Bradyrhizobium. We combined genome-wide analyses with a greenhouse inoculation study to investigate genomic diversity, heritability, and symbiosis trait variation among wild and early-domesticated cowpea genotypes. Cowpeas experienced modest decreases in genome-wide diversity during early domestication. Nonetheless, domesticated cowpeas responded efficiently to variation in symbiotic effectiveness, by forming more root nodules with nitrogen-fixing rhizobia and sanctioning nonfixing strains. Domesticated populations invested a larger proportion of host tissues into root nodules than wild cowpeas. Unlike soybean and wheat, cowpea showed no compelling evidence for degradation of symbiosis during domestication. Domesticated cowpeas experienced a less severe bottleneck than these crops and the low nutrient conditions in Africa where cowpea landraces were developed likely favored plant genotypes that gain substantial benefits from symbiosis. Breeders have largely neglected symbiosis traits, but artificial selection for improved plant responses to microbiota could increase plant performance and sustainability.
Purpose Crops rely on microbes for critical services, but host benefits can be influenced by local makeup of microbiota and the host’s capacity to select optimal strains. We investigated host benefits that cowpeas receive from microbiota depending on plant genotype, their domestication status, and soil source. Methods We performed a full factorial soil inoculation experiment. Twenty diverse cowpea genotypes, selected from wild and domesticated populations, were exposed to soil rinsates from four agricultural sites across California, all having cowpea cultivation and varied physicochemical features. Cowpea investment in and benefit from microbiota was quantified by measuring host growth response to inoculation, nodulation, and segregating trait variation. Results Variation in induction of root nodulation and strikingly heterogenous benefits to host growth were observed among soil sites. These effects were restricted to live soil inocula but were absent in autoclaved soil controls that lacked microbiota. Cowpeas expressed heritable variation in nodulation, but there was negligible effect of plant population or domestication status on the net benefit that hosts gained from microbiota. Conclusion Soils varied substantially and consistently among cultivation sites and were the most prominent driver shaping host growth effects on cowpeas. While growth benefits vary among host cultivars, soil microbiota (and the conditions that maintain them) predominantly shape plant performance in agricultural settings.
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