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

Abstract

word count: 237 words 19 Total word count: 5095 words 20 Abstract 21Genetic variation for partner quality in mutualisms is an evolutionary paradox. One possible 22 resolution to this puzzle is that there is a tradeoff between partner quality and other fitness-23 related traits. Here, we tested whether a susceptibility to parasitism is one such tradeoff in the 24 mutualism between legumes and nitrogen-fixing bacteria (rhizobia). We performed two 25 greenhouse experiments with the legume Medicago truncatula. In the first, we inoculated each 26 plant with the rhizobia Ensifer meliloti and with one of 40 genotypes of the parasitic root-knot 27 nematode Meloidogyne hapla. In the second experiment, we inoculated all plants with rhizobia 28 and half of the plants with a genetically variable population of nematodes. Using the number of 29 nematode galls as a proxy for infection severity, we found that plant genotypes differed in 30 susceptibility to nematode infection, and nematode genotypes differed in infectivity. Second, we 31 showed that there was a genetic correlation between the number of mutualistic structures formed 32 by rhizobia (nodules) and the number of parasitic structures formed by nematodes (galls). 33Finally, we found that nematodes disrupt the rhizobia mutualism: nematode-infected plants 34 formed fewer nodules and had less nodule biomass than uninfected plants. Our results 35 demonstrate that there is genetic conflict between attracting rhizobia and repelling nematodes in 36Medicago. If genetic conflict with parasitism is a general feature of mutualism, it could account 37 for the maintenance of genetic variation in partner quality and influence the evolutionary 38 dynamics of positive species interactions. 39 40 Impact summary 41Cooperative species interactions, known as mutualisms, are vital for organisms from plants to 42 humans. For example, beneficial microbes in the human gut are a necessary component of 43 digestive health. However, parasites often infect their hosts via mechanisms that are 44 extraordinarily similar to those used by mutualists, which may create a tradeoff between 45 attracting mutualists and resisting parasites. In this study, we investigated whether this tradeoff 46 exists, and how parasites impact mutualism function in the barrelclover Medicago truncatula, a 47 close relative of alfalfa. Legumes like Medicago depend on nitrogen provided by mutualistic 48 bacteria (rhizobia) to grow, but they are also infected by parasitic worms called nematodes, 49 which steal plant nutrients. Both microorganisms live in unique structures (nodules and galls) on 50 plant roots. We showed that the benefits of mutualism and the costs of parasitism are predicted 51 by the number of mutualistic structures (nodules) and the number of parasitic structures (galls), 52 respectively. Second, we found that there is a genetic tradeoff between attracting mutualists and 53 repelling parasites in Medicago truncatula: plant genotypes that formed more rhizobia nodules 54 also formed more nematode galls. Final...

Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism

“…plant-pollinator, plant-seed disperser) mutualisms, as well as other plant-biotic interactions (e.g. herbivores, parasites) that vary in niche breadth and effects on host fitness (Segraves & Anneberg, 2016;Wood et al, 2018). Although previous studies have demonstrated that most organisms interact with multiple mutualistic partners, the benefits of generalization and underlying mechanisms remained largely unresolved (Douglas, 1998;Heath & Stinchcombe, 2014).…”

Legacy of prior host and soil selection on rhizobial fitness in planta

“…Our understanding of how fluctuating selective environments shape rhizobial, and other bacterial, populations will be advanced by incorporating greater ecological realism and microbiome complexity in experiments (e.g., Wood et al. ); by designing experiments to tease apart the separate effects of soil, rhizosphere, and nodule selection on rhizobial populations; by conducting experiments for longer than two host generations; and by expanding the genomic diversity of host genotypes. Such experiments would not only advance our understanding of how selection affects microbial populations, but also may inform efforts to leverage beneficial plant–microbe interactions to increase agricultural yields and aid in ecosystem restoration (Gopalakrishnan et al.…”

Evolving together, evolving apart: measuring the fitness of rhizobial bacteria in and out of symbiosis with leguminous plants

“…A general understanding of how strain fitness, plant fitness and N fixation change with climate and land-use changes will require comprehensive experiments spanning legume systems. Future research should examine how additional direct and indirect biotic players, such as phages (Hashem & Angle, 1990), other competing bacteria (Xiao et al, 2017), arbuscular mycorrhizal fungi (Ossler et al, 2015), nematodes (Wood et al, 2018) and herbivores (Paudel & Bede, 2015) modify interactions between rhizobia and legumes. Such a systems-level approach will allow functional characterization of the interactions of specific community members and advance understanding of the natural history of microbes (Busby et al, 2017;Martiny & Walters, 2018).…”