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Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism.

ABSTRACT: Genetic variation for partner quality in mutualisms is an evolutionary paradox. One possible resolution to this puzzle is that there is a tradeoff between partner quality and other fitness-related traits. Here, we tested whether susceptibility to parasitism is one such tradeoff in the mutualism between legumes and nitrogen-fixing bacteria (rhizobia). We performed two greenhouse experiments with the legume Medicago truncatula. In the first, we inoculated each plant with the rhizobia Ensifer meliloti and with one of 40 genotypes of the parasitic root-knot nematode Meloidogyne hapla. In the second experiment, we inoculated all plants with rhizobia and half of the plants with a genetically variable population of nematodes. Using the number of nematode galls as a proxy for infection severity, we found that plant genotypes differed in susceptibility to nematode infection, and nematode genotypes differed in infectivity. Second, we showed that there was a genetic correlation between the number of mutualistic structures formed by rhizobia (nodules) and the number of parasitic structures formed by nematodes (galls). Finally, we found that nematodes disrupt the rhizobia mutualism: nematode-infected plants formed fewer nodules and had less nodule biomass than uninfected plants. Our results demonstrate that there is genetic conflict between attracting rhizobia and repelling nematodes in Medicago. If genetic conflict with parasitism is a general feature of mutualism, it could account for the maintenance of genetic variation in partner quality and influence the evolutionary dynamics of positive species interactions.

SUBMITTER: Wood CW

PROVIDER: S-EPMC6121810 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism.

Wood Corlett W CW Pilkington Bonnie L BL Vaidya Priya P Biel Caroline C Stinchcombe John R JR

Evolution letters 20180413 3

Genetic variation for partner quality in mutualisms is an evolutionary paradox. One possible resolution to this puzzle is that there is a tradeoff between partner quality and other fitness-related traits. Here, we tested whether susceptibility to parasitism is one such tradeoff in the mutualism between legumes and nitrogen-fixing bacteria (rhizobia). We performed two greenhouse experiments with the legume <i>Medicago truncatula</i>. In the first, we inoculated each plant with the rhizobia <i>Ens ...[more]

PMID: 30283679

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Project description:Background:Polyploidy is known to significantly alter plant genomes, phenotypes and interactions with the abiotic environment, yet the impacts of polyploidy on plant-biotic interactions are less well known. A particularly important plant-biotic interaction is the legume-rhizobia mutualism, in which rhizobia fix atmospheric nitrogen in exchange for carbon provided by legume hosts. This mutualism regulates nutrient cycles in natural ecosystems and provides nitrogen to agricultural environments. Despite the ecological, evolutionary and agricultural importance of plant polyploidy and the legume-rhizobia mutualism, it is not yet fully understood whether plant polyploidy directly alters mutualism traits or the consequences on plant growth. Scope:The aim was to propose a conceptual framework to understand how polyploidy might directly enhance the quantity and quality of rhizobial symbionts hosted by legume plants, resulting in increased host access to fixed nitrogen (N). Mechanistic hypotheses have been devised to examine how polyploidy can directly alter traits that impact the quantity (e.g. nodule number, nodule size, terminal bacteroid differentiation) and quality of symbionts (e.g. nodule environment, partner choice, host sanctions). To evaluate these hypotheses, an exhaustive review of studies testing the effects of plant polyploidy on the mutualism was conducted. In doing so, overall trends were synthesized, highlighting the limited understanding of the mechanisms that underlie variation in results achieved thus far, revealing striking gaps in knowledge and uncovering areas ripe for future research. Conclusions:Plant polyploidy can immediately alter nodule size, N fixation rate and the identity of rhizobial symbionts hosted by polyploid legumes, but many of the mechanistic hypotheses proposed here, such as bacteroid number and enhancements of the nodule environment, remain unexplored. Although current evidence supports a role of plant polyploidy in enhancing key aspects of the legume-rhizobia mutualism, the underlying mechanisms and effects on host benefit from the mutualism remain unresolved.

Dataset Information

Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism.

Publications

Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism.

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