Competitive interaction between non-nodulating and nodulating strains for nodulation of cowpea (<i>Vigna unguiculata</i>)

Singh, Inderpal; Ahmad, Mohammad

doi:10.1111/j.1574-6968.1991.tb04739.x

Cited by 4 publications

(4 citation statements)

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“…1a; Table 2). Our data are consistent with the results of previous reports of a reduction in nodulating strain fitness, measured by numbers of nodules formed by nodulating strains (22,23), but reveal that this does not always result in a significant decrease in all rhizobial fitness estimates (i.e., total nodule biomass). The higher ratio of nonnodulating strains in ecologically relevant UCR coinocula might explain this difference and further suggests a competitive role for nonnodulating strains at the root-soil interface, but we are unable to disentangle the effects of coinoculation ratios from any differences due to host genotype.…”

Section: Discussionsupporting

confidence: 82%

“…More specifically, the relative frequency of nonnodulating versus nodulating rhizobia also varies, but nonnodulating genotypes typically dominate and can encompass as much as 99% of the total rhizobial population (10)(11)(12)(13)(14)(15)(16)(17)(18). Nonnodulating strains can reduce the number of nodules formed by nodulating strains on legume hosts (22,23) and can invade nodule tissues in the presence of closely related nodulating strains (24,25). This suggests that they may be able to reduce nodulating strain fitness through competitive exclusion at the root surface.…”

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confidence: 99%

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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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Section: Discussionsupporting

confidence: 82%

mentioning

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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“…Notably the difference between these averages, 580 Kbp, is close to the size of symbiosis islands in fully sequenced Mesorhizobium genomes [49, 62]. Non-nodulating rhizobia that lack symbiosis islands or plasmids can suppress nodulation of host legumes by cooperative strains [77, 78], and diverse non-rhizobium microbiota regularly colonize healthy nodule tissue [79, 80]. In wild bradyrhizobia, uncooperative strains can co-found nodules with cooperative strains where they can have negative impacts on the fitness of both the host plant and the strain with which they co-invade [67].…”

Section: Discussionmentioning

confidence: 99%

Dynamic genomic architecture of mutualistic cooperation in a wild population of Mesorhizobium

et al. 2018

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Research on mutualism seeks to explain how cooperation can be maintained when uncooperative mutants co-occur with cooperative kin. Gains and losses of the gene modules required for cooperation punctuate symbiont phylogenies and drive lifestyle transitions between cooperative symbionts and uncooperative free-living lineages over evolutionary time. Yet whether uncooperative symbionts commonly evolve from within cooperative symbiont populations or from within distantly related lineages with antagonistic or free-living lifestyles (i.e., third-party mutualism exploiters or parasites), remains controversial. We use genomic data to show that genotypes that differ in the presence or absence of large islands of symbiosis genes are common within a single wild recombining population of Mesorhizobium symbionts isolated from host tissues and are an important source of standing heritable variation in cooperation in this population. In a focal population of Mesorhizobium, uncooperative variants that lack a symbiosis island segregate at 16% frequency in nodules, and genome size and symbiosis gene number are positively correlated with cooperation. This finding contrasts with the genomic architecture of variation in cooperation in other symbiont populations isolated from host tissues in which the islands of genes underlying cooperation are ubiquitous and variation in cooperation is primarily driven by allelic substitution and individual gene gain and loss events. Our study demonstrates that uncooperative mutants within mutualist populations can comprise a significant component of genetic variation in nature, providing biological rationale for models and experiments that seek to explain the maintenance of mutualism in the face of non-cooperators.

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“…It is also possible that non-nodulating rhizobia harm legumes by blocking infection of beneficial rhizobia. For instance, mutant non-nodulating strains have been experimentally shown to reduce nodulation by beneficial rhizobia during initial infection (Singh and Ahmad 1991). However, it is not clear from these short-term experiments whether host fitness is ultimately depressed by the presence of nonnodulating rhizobia.…”

Section: Non-nodulating Rhizobiamentioning

confidence: 99%

The origins of uncooperative rhizobia

Sachs¹,

Simms²

2008

Oikos

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Mutualisms are thought to be destabilized by exploitative mutants that receive benefits from partners without reciprocation. Nonetheless, there is surprisingly little evidence for the spread of exploitation in mutualist populations. In particular mutualisms, non‐beneficial partners are commonplace and this raises the question of whether exploitation is invading as an adaptive strategy. Here, we highlight the legume–rhizobium mutualism as a key test case. Rhizobial bacteria fix nitrogen in legume roots in exchange for carbon from their hosts. However, non‐beneficial rhizobia are widespread, including non‐fixing and non‐nodulating strains. Recent research has shown that legumes can punish some uncooperative rhizobia and substantially reduce their fitness, but these sanctions must not be universally effective. Important questions about uncooperative rhizobia remain unresolved. (1) Is it adaptive for rhizobia to be uncooperative with hosts? (2) Do uncooperative rhizobia evolve from cooperative ancestors? (3) What are the mechanisms of rhizobial exploitation? We describe experimental approaches and testable hypotheses that address these gaps in our knowledge.

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Competitive interaction between non-nodulating and nodulating strains for nodulation of cowpea (Vigna unguiculata)

Cited by 4 publications

References 10 publications

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

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

Dynamic genomic architecture of mutualistic cooperation in a wild population of Mesorhizobium

The origins of uncooperative rhizobia

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