Mutualistic rhizobia harbor genetic variation for traits related to parasite infection

Abstract

Nutritional mutualisms are defined by resource exchange, but growing evidence suggests that these interactions also shape resistance to parasites and pathogens. The evolutionary significance of this phenomenon is unclear, primarily because research has focused on mutualist-mediated plasticity rather than on mutualist contributions to heritable variation in the outcome of infection. To test whether nutritional mutualists harbor genetic variation for infection-related traits, we performed a quantitative genetic experiment in the nutritional mutualism between legumes and nitrogen-fixing rhizobia. We paired 10 mutualistic Sinorhizobium meliloti rhizobia strains with 20 Medicago truncatula plant genotypes in an incomplete factorial design, and experimentally infected plants with parasitic root-knot nematodes (Meloidogyne hapla). We used this design to estimate plant and rhizobia contributions to genetic variation in four infection-related traits: resistance, tolerance, virulence, and mutualism robustness to infection. Rhizobia contributed directly to genetic variation in virulence, and to parasite resistance and mutualism robustness via genotype-by-genotype interactions. Rhizobia did not contribute to genetic variation in tolerance. The effect of rhizobia on parasite resistance was partially explained by their effect on root growth. Our results raise the possibility that some nutritional mutualists play a role comparable to defensive mutualists in shaping the evolutionary potential of host defense traits. Teaser textNutritional mutualisms are everywhere. These mutualisms are defined by the exchange of resources between partners, but many have secondary effects on resistance to parasites, pathogens, or herbivores. Here, we show that a textbook nutritional mutualist (nitrogen-fixing rhizobia) harbors genetic variation for the hosts response to parasite infection. Our results imply that nutritional mutualists can impact the evolutionary potential of infection-related traits in their hosts, suggesting that these mutualisms may be overlooked drivers of defense evolution.