Root‐nodule Symbiosis: Molecular Basis of Nodule Formation

Abstract

Nutrient availability is a major limitation to plant growth. Legumes have entered into a symbiotic interaction with nitrogen‐fixing rhizobial bacteria that provide the plant with a source of nitrogen. The legume/rhizobial symbiosis is globally important for introducing nitrogen into biological systems. Legume crops are used in sustainable agricultural processes to naturally enrich the soil for nitrogen. Our understanding of the molecular mechanisms that underlie this interaction is expanding and we are beginning to understand the means by which the molecular dialogue occurs between the plant and the bacteria. The signalling pathway in the plant, that is responsible for the recognition of the bacterial signal Nod factor, appears to have evolved in part from a pre‐existing signalling pathway necessary for the establishment of the mycorrhizal symbiosis. Further research in this field may help to apply this symbiosis more broadly in agriculture.

Keywords: symbiosis; nodulation; legumes; rhizobia; signal transduction; calcium

Figure 1.

Legume responses to rhizobial bacteria. (a) Root hairs of Medicago truncatula grown in the presence of Nod factor. These cells normally grow straight, but in the presence of Nod factor show distorted growth and extensive root hair branches. (b) An infection thread originating from a curled and branched root hair. The rhizobial bacteria are stained blue inside the infection thread. The infection thread originates from root hair cells, but invades cortical cells of the root. Immediately below the infection thread, cortical cell division from inner cortical cells leads to the nodule primordium. (c) Fully developed nodules on the roots of M. truncatula from Oldroyd G (2001) Dissecting symbiosis: developments in nod factor signal transduction. Annals of Botany87: 709–718. Reproduced by permission of Annals of Botany Company.

Figure 2.

Nod factor of Sinorhizobium meliloti, the symbiont of alfalfa and M. truncatula. The basic Nod factor structure, common to all rhizobial bacteria, is a chitin backbone (black), with an N‐acyl (green) attached to the nonreducing terminal sugar. Additional modifications occur to this basic structure and these differ according to the species of rhizobia. In the case of S. meliloti, the N‐acyl group has 16 carbons in the chain with 2 double bonds, an acetyl group (red) attached to the nonreducing terminal sugar and a sulfate group (blue) attached to the reducing terminal sugar of the chitin backbone.

Figure 3.

Nod factor‐induced calcium spiking in root hair cells. (a) Root hair cells of M. truncatula injected with a calcium‐responsive dye allowing measurements of calcium via changes in florescence. The red coloration indicates high calcium levels: note the changes in calcium associated with the nuclei that represents a single calcium spike. (b) A graph showing florescence changes of a single cell undergoing Nod factor‐induced calcium changes. The first response, the large sustained calcium change is the calcium flux, which is rapidly followed by repetitive oscillations in the calcium levels that is calcium spiking.

Figure 4.

The Nod factor signalling pathway. The Nod factor signalling pathway defined by genetics in (a) M. truncatula and (b) Lotus japonicus. The genes are represented in boxes. The central part of this pathway is involved in both nodulation and mycorrhization.

Figure 5.

A model for Nod factor signalling. Two receptor‐like kinases, NFR1 and NFP/NFR5 (M. truncatula protein/L. japonicus protein), with two and three LysM domains, respectively, are required for Nod factor perception and an equivalent receptor‐like kinase is presumed to exist for recognition of a mycorrhizal signal. DMI2/SYMRK is an additional receptor‐like kinase with three leucine‐rich repeat domains that is a component of the common symbiosis‐signalling pathway. The phosphorylation cascade at the plasma membrane, following recognition by Nod factor, must be linked to induction of calcium changes associated with the nucleus. This probably involves the production of a secondary messenger. The nuclear pore is required to link Nod factor perception at the plasma membrane for the induction of calcium spiking and this may be involved in allowing entry of the secondary messenger into the nucleus. Calcium channels on the interior of the nuclear membrane and possibly the exterior of the nuclear envelope may be activated by the secondary messenger. Castor and Pollux, two putative cation channels from L. japonicus that are necessary for the induction of calcium spiking are located on the plastid. In contrast, the Pollux homologue in M. truncatula, DMI1, is located on the nuclear membrane. These putative cation channels may function as calcium channels or may be involved in the regulation of alternative cations. Calcium pumps that utilize ATP to move calcium against its concentration gradient must exist on the same membranes as the calcium channels and are required to refill the calcium store. The resultant calcium spikes in the nucleoplasm and nuclear‐associated cytoplasm activate CCaMK that is located in the nucleus. This calcium‐activated kinase regulates nodulin gene expression via the transcriptional regulators NSP1, NSP2 and ERN. A bifurcation in the common symbiosis signalling pathway exists downstream of CCaMK with a nodulation specific branch and presumably a mycorrhizal specific branch. Dashed lines indicate hypothetical interactions.

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References

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Further Reading

Oldroyd GE and Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nature Reviews. Molecular Cell Biology 5: 566–576.

Oldroyd G and Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9: 351–357.

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How to Cite close
Oldroyd, Giles(Sep 2007) Root‐nodule Symbiosis: Molecular Basis of Nodule Formation. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020128]