Rhizobium and Other N‐fixing Symbioses

Abstract

Nitrogen‐fixing symbioses between bacteria and plants are major nitrogen contributors to the terrestrial biosphere. The Rhizobium–legume interaction is the best known and is agronomically the most important one. Several alpha‐ and betaproteobacterial species (rhizobia) can infect legume roots via root hair or crack invasion, preceded by signal exchange in the rhizosphere and followed by signal transduction in the root, resulting in the construction of a nitrogen‐fixing root nodule. Actinorhizal nodule formation by members of the actinobacterial genus Frankia follows the same pattern but is less known in detail. The nitrogen‐fixing root symbioses have the same evolutionary origin as mycorrhizal symbioses. Cyanobacterial nitrogen‐fixing symbioses are more diversified and formed mainly with representatives of genus Nostoc, and occur in diverse plant groups, the best known being Azolla, Cycas and Gunnera. Whole‐genome sequencing of the microbial symbionts has revealed interesting features related to the genetics of signalling, genome architecture and biogeography.

Key Concepts:

  • Symbiotic nitrogen fixation in plants contributes significantly to terrestrial ecosystems and sustainable agriculture.

  • Symbiotic nitrogen‐fixing interactions arose several times during evolution.

  • The Rhizobium–legume symbiosis serves as a model and paradigm for other symbiotic interactions between bacteria and plants.

  • Nitrogen‐fixing root symbioses have an origin common with mycorrhizal symbioses.

  • Most rhizobia have well‐conserved nodulation genes which encode signals, nodulation factors, which are perceived by the plant.

  • Cyanobacterial symbioses with plants are diversified, but involve mainly one microbial genus, Nostoc.

Keywords: symbiosis; nitrogen fixation; plant–microbe interaction; Rhizobium; Frankia; cyanobacteria; infection; evolution; signalling; genomes

Figure 1.

Approximate order of historical events important for the evolution of nitrogen‐fixing symbioses, compiled from the sources Kistner and Parniske ; Lavin et al.; Osborne and Bergman ; Sprent ; Turner and Young and Wang et al. and references in them.

Figure 2.

Symbiotic nitrogen fixation in legumes is driven by solar energy acquired by photosynthesis of the plant and executed by the bacterial nitrogenase enzyme system. (a) A field with fodder galega (Galega orientalis) used for silage and as a bee plant. (b) Electron micrograph of free‐living Rhizobium galegae. (c) Indeterminate root nodule, coloured pink by the oxygen carrier leghaemoglobin. (d) Experiemental field of Astragalus sinicus with inoculated and uninoculated plots (from Biological Nitrogen Fixation with Emphasis on Legumes, Lindström K, EOLSS6.54.10.3, with permission from Eolss Publishers Co Ltd.). (e) Nodules containing bacteria that carry the reporter gene gusA, the product of which stains the nodule blue when a suitable substrate is added.

Figure 3.

Phylogenetic relationships in Leguminosae (left) and Nod factor structure (right). In the phylogenetic tree, taxa in bold face are dominated by nodulating species. The IRLC (inverted repeat‐lacking clade) comprises among others galegoid legumes the symbionts of which have been described as producing Nod factors with polyunsaturated fatty acids (frame on the left). Abbreviations for substitutions in Nod factor: Ac, acetyl; Ara, arabinosyl; Et, ethyl; Cb, carbamoyl; Fuc, fucosyl; G, N‐glycolyl; Gro, glyceryl; H, hydrogen; Man, mannosyl; Me, methyl and S, sulfate. Reprinted from Dresler‐Nurmi et al. with the permission of Springer‐Verlag..

Figure 4.

Bacterial infection. During root hair invasion infection threads initiate from infection foci and allow bacterial invasion of the cortex. Concomitant with these epidermal responses, cortical cells activate cell division to form the nodule meristem. During root hair entry, epidermal responses are associated with Nod factor perception that leads to gene expression via a calcium spiking‐dependent signalling pathway and root hair deformation via a signalling pathway independent of calcium spiking. During crack invasion the epidermis is breached and the bacteria gain direct access to cortical cells. Nod factor signalling is important in some species that undergo crack entry, but Nod factor‐independent crack invasion also exists and may be associated with rhizobial modification of cytokinins. Abbreviations: LHK1, Lotus histidine kinase; NSP1/NSP2, nodulation signalling pathway proteins; CCaMK, calcium/calmodulin‐dependent protein kinase; ENODs, early nodulation genes; NIN, nodule inception and LysM‐RLK, lysin motif receptor‐like kinase. After Oldroyd and Downie . Printed with the permission of ANNUAL REVIEWS, INC.

Figure 5.

Cyanobacteria in nitrogen‐fixing symbiosis. (a) Gunnera sp. (b) Gunnera gland with microsymbionts. (c) Cyanobacteria embedded in gland matrix. (d) Electron micrograph of section of cyanobactria inside gland. (e) Azolla filiculolides (Courtesy Department of Botany, University of Utrecht). (f) Cyanobacterial morphological types involved in symbiotic interactions. After Bergman et al.. Reprinted with the permission of Wiley‐Blackwell.

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Further Reading

Dessaux Y, Hinsinger P and Lemanceau P (eds) (2010) Rhizosphere: achievements and challenges. In: Developments in Plant and Soil Sciences, vol. 104, 535 pp. Berlin: Springer.

Franche C, Lindström K and Elmerich C (2009) Nitrogen‐fixing bacteria associated with leguminous and non‐leguminous plants. Plant and Soil 321: 35–39.

Lewis G, Schrire B, Mackinder B et al. (2005) Legumes of the World. UK Kew: Royal Botanic Gardens 577pp.

Masson‐Boivin C, Giraud E, Perret X et al. (2009) Establishing nitrogen‐fixing symbiosis with legumes: how many Rhizobium recipes? Trends in Microbiology 17(10): 458–466.

Pawlowski K (2009) Prokaryotic Symbionts in Plants, 306pp. Berlin, Heidelberg: Springer‐Verlag.

Rai AN, Bergman B and Rasmussen U (2002) Cyanobacteria in Symbiosis. Dordrecht, The Netherlands: Kluwer Academic Publishers 355pp.

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Lindström, Kristina, and Mousavi, Seyed Abdollah(Nov 2010) Rhizobium and Other N‐fixing Symbioses. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021157]