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Context dependence in the coevolution of plant and rhizobial mutualists.

ABSTRACT: Several mechanisms are expected to rapidly rid mutualisms of genetic variation in partner quality. Variation for mutualist quality, however, appears to be widespread. We used a model legume-rhizobium mutualism to test for evidence that context-dependent selection may maintain variation in partner quality. In a greenhouse experiment using 10 natural populations of Medicago truncatula and two strains of Sinorhizobium medicae, we detected significant genotype x genotype (G x G) interactions for plant fitness, indicating that the most beneficial rhizobium strain depends on the host genotype. In a second experiment using a subset of the plant populations used in the first experiment, we detected significant G x G interactions for both plant and rhizobium fitness. Moreover, the plant population with which rhizobium strains gained the greatest benefit depended on the nitrogen environment. Finally, we found that in a high nitrogen environment, all plant populations had lower fitness when inoculated with a 1:1 mixture of strains than with the worse single strain alone, suggesting that nitrogen shifts the exchange of benefits in favour of rhizobia. Our data suggest that genotype, nitrogen and biotic dependency might contribute to the maintenance of genetic variation in mutualist quality when coupled with spatial or temporal heterogeneity in the environment.

SUBMITTER: Heath KD

PROVIDER: S-EPMC2270936 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti-Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.

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Context dependence in the coevolution of plant and rhizobial mutualists.

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