Blog
About

9
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N 2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis–Mimosa pudica system. N 2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N 2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N 2-fixation mutualistic trait.

          eLife digest

          Rhizobia are soil bacteria that are able to form a symbiotic relationship with legumes – plants that include peas, beans and lentils. The bacteria move into cells in the roots of the plant and cause new organs called nodules to form. Inside the nodules the bacteria multiply before being released to the soil again. Also while in the nodules, the bacteria receive carbon-containing compounds from the plant. In return many of the bacteria convert (or “fix”) nitrogen from the air into compounds that the plant can use to build molecules such as DNA and proteins. Yet, some of the bacteria are “non-fixers” that provide little or no benefit to the host plant.

          Evidence suggests that legumes select against non-fixer bacteria, though it was not clear when or how this selection process occurs. Daubech, Remigi et al. have now followed the number and viability of two variants of a bacteria species called Cupriavidus taiwanensis as they form a symbiotic interaction with Mimosa pudica, a member of the pea family. The two types of bacteria differed only by whether or not they were able to fix nitrogen. At first fixers and non-fixers entered nodules and multiplied at equal rates. Later, the fixers progressively outcompeted the non-fixers. Then, around 20 days after the bacteria entered the plant, nodule cells that contained non-fixers degenerated. This indicates that the nodule cells help to control bacterial proliferation based on the benefits they receive in return.

          Further experiments and mathematical modeling also showed that over repeated cycles of root nodule formation, nitrogen fixers can invade a bacterial population dominated by non-fixer bacteria. The likelihood that this invasion will be successful increases as three other factors increase: the proportion of fixer bacteria in the initial population, the number of available plants, and the length of time the bacteria spend in the nodules. This mechanism ensures the maintenance and spread of nitrogen-fixing traits in the bacterial population.

          Improving the processes of biological nitrogen fixation could help to reduce the amount of fertilizers required to grow crops. This in the future could help make agricultural ecosystems more sustainable. The results presented by Daubech, Remigi et al. provide guidelines that could be used to select nitrogen-fixing bacteria on legume crops or on nitrogen-fixing cereals that may be engineered in the future. Further work is now needed to understand in more detail the molecular mechanisms that lead to the death of non-fixer bacteria.

          Related collections

          Most cited references 51

          • Record: found
          • Abstract: found
          • Article: not found

          Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.

          pRK212.2, a derivative of the broad host range plasmid RK2, contains two EcoRI cleavage fragments, A and B, neither of which can replicate by itself in Escherichia coli. Fragment A (41.7 kilobases), but not fragment B (14.4 kilobases), can be cloned by insertion into the unrelated plasmids mini-F and ColE1. Fragment B contains the origin of replication and the ampicillin-resistance determinant of RK2. Transformation of E. coli cells containing the mini-F-fragment A hybrid plasmid with fragment B DNA results in the recircularization and replication of fragment B as a nonmobilizable plasmid (pRK2067) with the copy number and incompatibility properties of RK2. Fragment B cannot be cloned in the absence of fragment A because the latter fragment suppresses a function, specified by fragment B, that results in loss of host cell viability. A small segment (2.4 kilobases) of fragment B that contains the RK2 origin of replication but no longer affects host cell growth in the absence of fragment A had been cloned previously by insertion into a ColE1 plasmid. This hybrid plasmid, designated pRK256, will replicate in E. coli polA mutants only when a fragment A-bearing helper plasmid is present. These results demonstrate that the potentially lethal function specified by fragment B of RK2 is not necessary for replication and that at least one trans-acting function is directly involved in RK2 replication.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases.

            Although most higher plants establish a symbiosis with arbuscular mycorrhizal fungi, symbiotic nitrogen fixation with rhizobia is a salient feature of legumes. Despite this host range difference, mycorrhizal and rhizobial invasion shares a common plant-specified genetic programme controlling the early host interaction. One feature distinguishing legumes is their ability to perceive rhizobial-specific signal molecules. We describe here two LysM-type serine/threonine receptor kinase genes, NFR1 and NFR5, enabling the model legume Lotus japonicus to recognize its bacterial microsymbiont Mesorhizobium loti. The extracellular domains of the two transmembrane kinases resemble LysM domains of peptidoglycan- and chitin-binding proteins, suggesting that they may be involved directly in perception of the rhizobial lipochitin-oligosaccharide signal. We show that NFR1 and NFR5 are required for the earliest physiological and cellular responses to this lipochitin-oligosaccharide signal, and demonstrate their role in the mechanism establishing susceptibility of the legume root for bacterial infection.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              The evolution of mutualisms: exploring the paths between conflict and cooperation.

              Mutualisms are of fundamental importance in all ecosystems but their very existence poses a series of challenging evolutionary questions. Recently, the application of molecular analyses combined with theoretical advances have transformed our understanding of many specific systems, thereby contributing to the possibility of a more general understanding of the factors that influence mutualisms.
                Bookmark

                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                12 October 2017
                2017
                : 6
                Affiliations
                [1 ]deptThe Laboratory of Plant-Microbe Interactions Université de Toulouse, INRA, CNRS Castanet-TolosanFrance
                [2 ]deptNew Zealand Institute for Advanced Study Massey University AucklandNew Zealand
                [3 ]Fédération de Recherches Agrobiosciences, Interactions et Biodiversité, Plateforme d’Imagerie TRI, CNRS - UPS Castanet-TolosanFrance
                [4 ]deptResearch Group for Theoretical Models of Eco-evolutionary Dynamics, Department of Evolutionary Theory Max Planck Institute for Evolutionary Biology PlönGermany
                Fred Hutchinson Cancer Research Center United States
                Fred Hutchinson Cancer Research Center United States
                Author notes
                [†]

                These authors contributed equally to this work.

                Article
                28683
                10.7554/eLife.28683
                5687860
                29022875
                © 2017, Daubech et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                Product
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-12-ADAP-0014-01
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100006488, Institut National de la Recherche Agronomique;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004189, Max-Planck-Gesellschaft;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-16-CE20-0011-01
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-10-LABX-41
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-11-IDEX-0002-02
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Genomics and Evolutionary Biology
                Custom metadata
                Experiments and mathematical modelling show that rare nitrogen fixing symbionts invade a population dominated by non-fixing bacteria across plant generations, above a threshold of a combination of ecological factors.

                Life sciences

                other, evolution, nitrogen fixation, symbiosis, rhizobium

                Comments

                Comment on this article