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Conditional sanctioning in a legume-Rhizobium mutualism.

ABSTRACT: Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually house multiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settings, while intermediate fixers are common. Here, we modeled how plants should respond to an intermediate fixer that was otherwise isogenic and tested model predictions using pea plants. Intermediate fixers were only tolerated when a better strain was not available. In agreement with model predictions, nodules containing the intermediate-fixing strain were large and healthy when the only alternative was a nonfixer, but nodules of the intermediate-fixing strain were small and white when the plant was coinoculated with a more effective strain. The reduction in nodule size was preceded by a lower carbon supply to the nodule even before differences in nodule size could be observed. Sanctioned nodules had reduced rates of nitrogen fixation, and in later developmental stages, sanctioned nodules contained fewer viable bacteria than nonsanctioned nodules. This indicates that legumes can make conditional decisions, most likely by comparing a local nodule-dependent cue of nitrogen output with a global cue, giving them remarkable control over their symbiotic partners.

SUBMITTER: Westhoek A

PROVIDER: S-EPMC8126861 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Conditional sanctioning in a legume-<i>Rhizobium</i> mutualism.

Westhoek Annet A Clark Laura J LJ Culbert Michael M Dalchau Neil N Griffiths Megan M Jorrin Beatriz B Karunakaran Ramakrishnan R Ledermann Raphael R Tkacz Andrzej A Webb Isabel I James Euan K EK Poole Philip S PS Turnbull Lindsay A LA

Proceedings of the National Academy of Sciences of the United States of America 20210501 19

Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually house multiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settin ...[more]

PMID: 33941672

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Project description:UnlabelledRhizobia are best known for nodulating legume roots and fixing atmospheric nitrogen for the host in exchange for photosynthates. However, the majority of the diverse strains of rhizobia do not form nodules on legumes, often because they lack key loci that are needed to induce nodulation. Nonnodulating rhizobia are robust heterotrophs that can persist in bulk soil, thrive in the rhizosphere, or colonize roots as endophytes, but their role in the legume-rhizobium mutualism remains unclear. Here, we investigated the effects of nonnodulating strains on the native Acmispon-Bradyrhizobium mutualism. To examine the effects on both host performance and symbiont fitness, we performed clonal inoculations of diverse nonnodulating Bradyrhizobium strains on Acmispon strigosus hosts and also coinoculated hosts with mixtures of sympatric nodulating and nonnodulating strains. In isolation, nonnodulating Bradyrhizobium strains did not affect plant performance. In most cases, coinoculation of nodulating and nonnodulating strains reduced host performance compared to that of hosts inoculated with only a symbiotic strain. However, coinoculation increased host performance only under one extreme experimental treatment. Nearly all estimates of nodulating strain fitness were reduced in the presence of nonnodulating strains. We discovered that nonnodulating strains were consistently capable of coinfecting legume nodules in the presence of nodulating strains but that the fitness effects of coinfection for hosts and symbionts were negligible. Our data suggest that nonnodulating strains most often attenuate the Acmispon-Bradyrhizobium mutualism and that this occurs via competitive interactions at the root-soil interface as opposed to in plantaImportanceRhizobia are soil bacteria best known for their capacity to form root nodules on legume plants and enhance plant growth through nitrogen fixation. Yet, most rhizobia in soil do not have this capacity, and their effects on this symbiosis are poorly understood. We investigated the effects of diverse nonnodulating rhizobia on a native legume-rhizobium symbiosis. Nonnodulating strains did not affect plant growth in isolation. However, compared to inoculations with symbiotic rhizobia, coinoculations of symbiotic and nonnodulating strains often reduced plant and symbiont fitness. Coinoculation increased host performance only under one extreme treatment. Nonnodulating strains also invaded nodule interiors in the presence of nodulating strains, but this did not affect the fitness of either partner. Our data suggest that nonnodulating strains may be important competitors at the root-soil interface and that their capacity to attenuate this symbiosis should be considered in efforts to use rhizobia as biofertilizers.

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

Conditional sanctioning in a legume-Rhizobium mutualism.

Publications

Conditional sanctioning in a legume-<i>Rhizobium</i> mutualism.

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