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  • Review Article
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How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

Nature Reviews Microbiology volume 5, pages 619–633 (2007)Cite this article

Key Points

  • Symbiotic nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which it enters the plant root.

  • Once these invasion structures reach the target cells in the interior of the plant root, the bacteria are endocytosed within a host cell membrane-derived compartment.

  • In the microaerobic environment provided by the host cell, the bacteria differentiate into a specialized form called a bacteroid. The bacteroid form expresses the oxygen-sensitive enzyme nitrogenase that catalyzes the conversion of atmospheric nitrogen to ammonia.

  • The dissection of the bacterial and plant signalling pathways that are involved in each stage of the invasion process has been facilitated by the complete genomic sequencing of Sinorhizobium meliloti and the near complete sequencing of the genome of the model host plant Medicago truncatula.

  • Rhizobial bacteria interact very differently with the plant innate immune system than other groups of bacteria. Rhizobia lack some of the microbial molecular patterns that provoke plant defence responses. Additionally, legume plants differ from other plant families in that they lack the ability to perceive and respond defenceively to other microbial molecular patterns.

  • Symbiotic rhizobial bacteria are similar to pathogenic bacteria such as Brucella spp, in that they both form chronic infections of eukaryotic cells within a host-derived membrane compartment, and require some of the same bacterial factors for survival within the host. These factors include the correct structure of the lipopolysaccharide core and lipid A, presence of cyclic β-glucans, and a common bacterial regulatory circuitry.

Abstract

Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).

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Figure 1: The initial signalling dialogue between Sinorhizobium meliloti and Medicago truncatula.
Figure 2: Downstream components of the Nod factor signal transduction system.
Figure 3: Root hair invasion by Sinorhizobium meliloti.
Figure 4: Infection thread failure can be caused by plant or bacterial defects.
Figure 5: Endocytosis of bacteria and bacteroid differentiation.

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Acknowledgements

We are very grateful to B. K. Minesinger, S. M. Simon, R. V. Woodruff and the reviewers for their helpful comments. We would like to thank members of the Walker laboratory for helpful discussions, and the National Institutes of Health (USA), the Japan Society for the Promotion of Science, the National Science and Research Council of Canada, and the Jane Coffin Childs Fund for Medical Research for funding. G. C. W. is an American Cancer Society Research Professor.

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  1. Department of Biology, Massachusetts Institute of Technology, Building 68, Room 633, 77 Massachusetts Avenue, Cambridge, 02139, Massachusetts, USA

    Kathryn M. Jones, Hajime Kobayashi, Bryan W. Davies, Michiko E. Taga & Graham C. Walker

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DATABASES

Entrez Genome Project

Lotus japonicus

Medicago sativa

Medicago truncatula

Sinorhizobium meliloti

Entrez Protein

Nod D1

Nod D2

Nod D3

FURTHER INFORMATION

Graham C. Walker's homepage

Glossary

Flavonoid

A 2-phenyl-1,4-benzopyrone derivative, produced by plants, that serves as a defence and signalling compound.

Nod factor

A lipochitooligosaccharide compound that induces multiple responses that are required for nodulation of appropriate host plants.

Symbiotic exopolysaccharide

A rhizobial secreted β-glucan that is structurally distinct for different species and that mediates infection thread formation.

Infection thread

An ingrowth of the root hair cell membrane, populated with rhizobial bacteria, that progresses inward by new membrane synthesis at the tip.

Symbiosome

A host-derived membrane compartment that originates from the infection thread housing a bacteroid.

Bacteroid

A rhizobial bacterium that has been endocytosed by a plant cell and has elongated and/or branched, and has differentiated or is differentiating into a form that can perform nitrogen fixation.

Nitrogen fixation

The reduction of atmospheric dinitrogen to ammonia.

Colonized curled root hair

A root hair that has been induced by Nod factor to curl around a microcolony of rhizobial bacteria and entrap it.

Auxin

A plant hormone (chiefly indole acetic acid) that regulates plant growth in a concentration-dependent manner.

Nodule primordium

Dedifferentiated, proliferating tissue that develops in the plant cortex during nodule initiation.

Cyclic β-glucan

A cyclized β-1,2 chain of 17–25 glucose residues produced by rhizobial bacteria, Brucella spp. and Agrobacterium spp. that localizes to the periplasm and that functions in osmotolerance and in interaction with host membranes.

Succinoglycan

A symbiotic exopolysaccharide produced by S. meliloti, also known as EPS I, that mediates infection thread formation. An octasaccharide repeating unit modified with acetyl, succinyl and pyruvyl substituents that can be polymerized into a high molecular weight or a low molecular weight form composed of monomers, dimers and trimers.

Galactoglucan

A second exopolysaccharide of S. meliloti (EPS II) that can mediate infection thread formation on M. sativa at a low efficiency and that is produced when an intact copy of the ExpR regulator is present. A disaccharide repeating unit modified with acetyl and pyruvyl substituents.

Endoreduplication

Genomic replication without cytokinesis that results in greater than 2n DNA content within a cell.

Indeterminate nodule

A nodule formed by plants of some clades of legumes that develops a continuously growing nodule meristem at the distal end and has zones of tissue at different stages of development.

α -proteobacteria

A group of bacteria that contains several species able to persist within host-derived membrane-bound compartments in eukaryotic cells. Includes rhizobial bacteria and mammalian pathogens such as Brucella spp., Bartonella spp. and Rickettsia spp.

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Jones, K., Kobayashi, H., Davies, B. et al. How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5, 619–633 (2007). https://doi.org/10.1038/nrmicro1705

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