Selection for cheating across disparate environments in the legume‐rhizobium mutualism

Porter, Stephanie S.; Simms, Ellen L.

doi:10.1111/ele.12318

Cited by 92 publications

(106 citation statements)

References 55 publications

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“…For example, there is likely to be an energetic cost to AM fungi for acquiring, transporting, and delivering P to the host. As a result of these costs, one would expect a tradeoff between symbiont growth rate per unit carbon (C) and mutualistic ability, as has been observed in AM fungi (Bever, ; Bennett & Bever, ; Bever et al ., ) and rhizobia (Porter & Simms, ). Given this tradeoff, the least beneficial symbiont would have the highest rate of increase and the mutualism would be expected to evolve toward parasitism in a well‐mixed system.…”

Section: Descriptionmentioning

confidence: 99%

Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts

2015

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SummaryThe common occurrence of mutualistic interactions between plants and root symbionts is problematic. As the delivery of benefit to hosts involves costs to symbionts, symbionts that provide reduced benefit to their host are expected to increase in frequency. Plants have been shown to allocate preferentially to the most efficient symbiont and this preferential allocation may stabilize the mutualism.I construct a general model of the interactive feedbacks of host preferential allocation and the dynamics of root symbiont populations to evaluate the stability of nutritional mutualisms.Preferential allocation can promote the evolution of mutualism even when the cost to the symbiont is very large. Moreover, the physiological plasticity of preferential allocation likely leads to coexistence of beneficial and nonbeneficial symbionts. For arbuscular mycorrhizal fungi, which facilitate plant uptake of phosphorus (P), the model predicts greater P transfer from these fungi per unit carbon invested with decreasing concentrations of soil P and with increasing concentrations of atmospheric CO 2 , patterns that have been observed in laboratory and field studies.This framework connects physiological plasticity in plant allocation to population processes that determine mutualism stability and, as such, represents a significant step in understanding the stability and environmental patterns in mutualism.

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Section: Descriptionmentioning

confidence: 99%

Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts

2015

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“…This symbiosis has become a key model for mutualism evolution, given the relative ease with which rhizobium genetic variants can be isolated and subsequently manipulated in experiments to test key predictions of evolutionary theory [10][11][12][13][14]. This recent boom in studies of phenotypic evolution in rhizobia, a long history of molecular genetic investigation resulting in well-annotated reference genomes (e.g.…”

Section: Introductionmentioning

confidence: 99%

Ecological genomics of mutualism decline in nitrogen-fixing bacteria

2016

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Anthropogenic changes can influence mutualism evolution; however, the genomic regions underpinning mutualism that are most affected by environmental change are generally unknown, even in well-studied model mutualisms like the interaction between legumes and their nitrogen (N)-fixing rhizobia. Such genomic information can shed light on the agents and targets of selection maintaining cooperation in nature. We recently demonstrated that N-fertilization has caused an evolutionary decline in mutualistic partner quality in the rhizobia that form symbiosis with clover. Here, population genomic analyses of N-fertilized versus control rhizobium populations indicate that evolutionary differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) contributes to partner quality decline. Moreover, patterns of genetic variation at selected loci were consistent with recent positive selection within N-fertilized environments, suggesting that N-rich environments might select for less beneficial rhizobia. By studying the molecular population genomics of a natural bacterial population within a long-term ecological field experiment, we find that: (i) the N environment is indeed a potent selective force mediating mutualism evolution in this symbiosis, (ii) natural variation in rhizobium partner quality is mediated in part by key symbiosis genes on the symbiotic plasmid, and (iii) differentiation at selected genes occurred in the context of otherwise recombining genomes, resembling eukaryotic models of adaptation.

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“…1a and b; Table 2). Legumes have finely tuned mechanisms to regulate nodule numbers (46), but the number of nodules formed in any interaction is nonetheless a product of the host and rhizobium genotypes (38,47). This suggests that host control over nodule numbers is incomplete (34).…”

Section: Discussionmentioning

confidence: 99%

Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism

Gano-Cohen

Stokes

Blanton

et al. 2016

Appl Environ Microbiol

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Rhizobia 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 planta. IMPORTANCERhizobia 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. Rhizobia are heterotrophic soil bacteria with diverse lifestyles. Some rhizobial lineages have acquired the capacity to form nodules on legume roots and fix atmospheric nitrogen for these hosts (1). Nodulating rhizobia are attracted to flavonoids released by legumes. In response, t...

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Selection for cheating across disparate environments in the legume‐rhizobium mutualism

Cited by 92 publications

References 55 publications

Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts

Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts

Ecological genomics of mutualism decline in nitrogen-fixing bacteria

Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism

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