Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?

Masson‐Boivin, Catherine; Giraud, Éric; Perret, Xavier; Batut, Jacques

doi:10.1016/j.tim.2009.07.004

Cited by 506 publications

(354 citation statements)

References 79 publications

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“…An evolutionary perspective suggests that it might be especially profitable to find and study mechanisms underlying natural polymorphisms in functionally relevant genes. Functional genetic studies of nitrogen fixation (Masson-Boivin et al 2009) and cellular interactions between plant and rhizobium cells Prell et al 2009) should be conducted with an eye toward uncovering such variability in rhizobial populations. Once control traits have been identified, our model makes a number of specific predictions about the outcome of the mutualism as a function of different combinations of traits.…”

Section: Rhizobium Traits and Empirical Questionsmentioning

confidence: 99%

“…Rhizobia are soil-dwelling alpha-and beta-proteobacteria that form nitrogen-fixation symbioses with many legumes (Sprent 2007;Masson-Boivin et al 2009). Rhizobia infect legume roots, stimulate hosts to produce nodules, and differentiate into specialized endosymbiotic cells called bacteroids, which reduce atmospheric dinitrogen in exchange for plant photosynthates (Trainer and Charles 2006;Prell et al 2009).…”

Section: Introductionmentioning

confidence: 99%

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Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium Mutualism

Akçay

Simms

2011

The American Naturalist

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Two important questions about mutualisms are how the fitness costs and benefits to the mutualist partners are determined and how these mechanisms affect the evolutionary dynamics of the mutualism. We tackle these questions with a model of the legumerhizobium symbiosis that regards the mutualism outcome as a result of biochemical negotiations between the plant and its nodules. We explore the fitness consequences of this mechanism to the plant and rhizobia and obtain four main results. First, negotiations permit the plant to differentially reward more-cooperative rhizobia-a phenomenon termed "plant sanctions"-but only when more-cooperative rhizobia also provide the plant with good outside options during negotiations with other nodules. Second, negotiations may result in seemingly paradoxical cases where the plant is worse off when it has a "choice" between two strains of rhizobia than when infected by either strain alone. Third, even when sanctions are effective, they are by themselves not sufficient to maintain cooperative rhizobia in a population: less cooperative strains always have an advantage at the population level. Finally, partner fidelity feedback, together with genetic correlations between a rhizobium strain's cooperativeness and the outside options it provides, can maintain cooperative rhizobia. Our results show how joint control over the outcome of a mutualism through the proximate mechanism of negotiation can affect the evolutionary dynamics of interspecific cooperation. Disciplines Biology | Developmental Biology | Evolution CommentsAt the time of publication, author Erol Akçay was affiliated with the University of Tennessee. Currently, he is a faculty member at the Department of Biology at the University of Pennsylvania. Online enhancements: appendix, Mathematica file.abstract: Two important questions about mutualisms are how the fitness costs and benefits to the mutualist partners are determined and how these mechanisms affect the evolutionary dynamics of the mutualism. We tackle these questions with a model of the legumerhizobium symbiosis that regards the mutualism outcome as a result of biochemical negotiations between the plant and its nodules. We explore the fitness consequences of this mechanism to the plant and rhizobia and obtain four main results. First, negotiations permit the plant to differentially reward more-cooperative rhizobia-a phenomenon termed "plant sanctions"-but only when more-cooperative rhizobia also provide the plant with good outside options during negotiations with other nodules. Second, negotiations may result in seemingly paradoxical cases where the plant is worse off when it has a "choice" between two strains of rhizobia than when infected by either strain alone. Third, even when sanctions are effective, they are by themselves not sufficient to maintain cooperative rhizobia in a population: less cooperative strains always have an advantage at the population level. Finally, partner fidelity feedback, together with genetic correlations between a rhizobium strain...

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Section: Rhizobium Traits and Empirical Questionsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium Mutualism

Akçay

Simms

2011

The American Naturalist

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“…In contrast to legumes, which are monophyletic (Werner et al 2014), molecular techniques have demonstrated that rhizobia are polyphyletic, belonging to diverse bacterial genera of the Alphaproteobacteria and Betaproteobacteria (Masson-Boivin et al 2009). In RNB, symbiotic ability is conferred by genes for nodulation and nitrogen fixation that can be acquired via lateral transfer of plasmids or genomic islands (Broughton 2003;Freiberg et al 1997;Moulin et al 2004;Nandasena et al 2007;Sullivan and Ronson 1998).…”

Section: Introductionmentioning

confidence: 99%

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Ziegler

Pothier

Ardley

et al. 2015

Appl Microbiol Biotechnol

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Accurate identification of soil bacteria that form nitrogen-fixing associations with legume crops is challenging given the phylogenetic diversity of root nodule bacteria (RNB). The labor-intensive and time-consuming 16S ribosomal RNA (rRNA) sequencing and/or multilocus sequence analysis (MLSA) of conserved genes so far remain the favored molecular tools to characterize symbiotic bacteria. With the development of mass spectrometry (MS) as an alternative method to rapidly identify bacterial isolates, we recently showed that matrix-assisted laser desorption ionization (MALDI) time-of-flight (TOF) can accurately characterize RNB found inside plant nodules or grown in cultures. Here, we report on the development of a MALDI-TOF RNB-specific spectral database built on whole cell MS fingerprints of 116 strains representing the major rhizobial genera. In addition to this RNB-specific module, which was successfully tested on unknown field isolates, a subset of 13 ribosomal proteins extracted from genome data was found to be sufficient for the reliable identification of nodule isolates to rhizobial species as shown in the putatively ascribed ribosomal protein masses (PARPM) database. These results reveal that data gathered from genome sequences can be used to expand spectral libraries to aid the accurate identification of bacterial species by MALDI-TOF MS.

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“…Legumes and soil bacteria collectively known as rhizobia have coevolved a mutualistic endosymbiosis of major ecological importance that contributes ca 25% of global nitrogen cycling (Masson-Boivin et al, 2009). Rhizobia elicit on legume roots -occasionally stems-the formation of specialized organs called nodules in which they fix nitrogen to the benefit of the plant.…”

Section: Introductionmentioning

confidence: 99%

“…Symbiotic traits have been disseminated over large phylogenetic distances as extant rhizobial lineages diverged long before they acquired symbiotic properties (Turner and Young, 2000), that is, after legumes appeared on earth 60 million years ago (Sprent, 2007). In the many cases where the donor and recipient bacteria were phylogenetically or genetically distant, expression of the symbiotic potential brought by LGT may have required genomic remodeling (Masson-Boivin et al, 2009;Marchetti et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?

Cited by 506 publications

References 79 publications

Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium Mutualism

Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium Mutualism

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Experimental evolution of nodule intracellular infection in legume symbionts

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