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Plant–microbe interactions

A receptor in symbiotic dialogue

Naturevolume 417pages910911 (2002) | Download Citation

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Proteins that help plants connect with symbiotic microbes have been identified. These proteins are related to receptors in animals and plants that function in the innate immune system and organ development.

Many plants can grow on soils that are poor in nutrients, and they do so by forming symbiotic associations with microbes. These associations require a molecular dialogue between the two partners. On pages 959 and 962 of this issue, Stracke et al.1 and Endre et al.2 describe how they have identified genes that encode a plant protein that is essential to the dialogue.

Important examples of microbes involved in symbiosis are bacteria called rhizobia and fungi — 'arbuscular mycorrhizal fungi' — that respectively supply the plant host with nitrogen- and phosphorus-containing nutrients3,4. In return, the microbes receive carbohydrate nutrients from the plant. The genes identified by Stracke et al. and Endre et al. seem to belong to a large family of plant and animal genes that encode a particular class of receptor proteins. These proteins are characterized by having a repeated motif rich in the amino acid leucine — called a leucine-rich-repeat (LRR) — in an extracellular domain5,6,7. In animals the proteins comprise a group, known as the Toll-like receptors, that function in the innate immune system8. In plants they belong to a subfamily that has in common an intracellular serine/threonine kinase domain that triggers a signalling cascade inside the cell. Several members of this plant subfamily are involved in defence against pathogenic microbes, or in shoot development9 (Fig. 1).

Figure 1: Comparison of members of the protein family of receptors containing extracellular leucine-rich-repeats (LRR).
Figure 1

This tree of protein relatedness compares examples from various subfamilies in animals and plants, and indicates the breadth of species in which the receptors are found, and the variety of functions that they have. The receptors' involvement in plant–microbe interactions, as a component of the plant side of the molecular dialogue in symbiosis, is described by Stracke et al.1 and Endre et al.2 in this issue. The plants concerned are the model legumes Lotus japonicus, Medicago sativa and Medicago truncatula, and the pea (Pisum sativum). The examples not referenced above are reviewed in refs 6 and 8. For zebrafish, the assignment is based on data (BG304206) submitted to Genbank by S. Johnson. CLAVATA1 is the receptor that recognizes CLAVATA3.

It is not too surprising that receptors involved in plant–microbe symbiosis belong to the LRR receptor subfamily, given that it is one of the largest groups of receptors in the plant kingdom with, for instance, 174 members in the 'model' plant Arabidopsis alone10. But it is surprising that Stracke et al. and Endre et al. found a function for a highly similar LRR receptor in different plant species — not only in the model legumes Lotus japonicus, Medicago sativa and Medicago truncatula, but also in the agriculturally important crop plant, pea (Pisum sativum). In all, the two groups carried out a genetic analysis of nine mutants that have defects in the early stages of symbiosis, discovering the involvement of a member of the LRR receptor family and by implication its key role in symbiosis.

For the rhizobium–plant interaction, various signal molecules produced by the microbial partner have been identified. One group — the Nod factors — has attracted much attention because Nod factors specifically trigger the host plants (belonging exclusively to the legume family) to produce a specialized microbe-accommodating organ, the root nodule3. But little is known of the plant factors that recognize rhizobial signal molecules. And even less is known of plant interactions with arbuscular mycorrhiza: for this microbe, no signal molecules have been identified.

In finding a receptor protein involved in recognizing signal molecules from both rhizobia bacteria and arbuscular mycorrhiza, Stracke et al.1 and Endre et al.2 have provided a long-awaited breakthrough. Identifying the genetic basis of microbial recognition in the plant hosts has been hampered by technical difficulties, which are especially acute for plants that form strong symbiotic relationships. As exemplified by legumes, such plants have relatively large genomes, which in some cases exceed the size of the human genome. That makes identification of point mutations — single-nucleotide changes in DNA — extremely difficult. Furthermore, in plants, gene-knockout techniques are still in their infancy11,12. Stracke et al. and Endre et al. circumvented these difficulties by making optimal use of the advantages offered by classical plant genetics in legumes — the production of large numbers of mutants and genome-map-based cloning — and the increased availability of nucleotide sequence data.

The results open the way for detailed analysis of the direct binding partners, and downstream signalling pathways, that are associated with microbial recognition. Such analysis may soon provide further insight into the similarities with signal pathways involving other classes of LRR receptor, and could reveal connections with the recognition mechanism of factors produced by pathogenic microbes or signalling peptides involved in development.

The future bottleneck in studying this receptor family is our lack of knowledge about the signal molecules that are recognized by the receptors. Up to now, a triggering factor has been identified for only two plant LRR receptor proteins. These factors (microbial flagellin5 and the plant differentiation factor called CLAVATA3) are extracellular proteins. The structural evidence is consistent with the idea that LRR sequence motifs have a general function in protein recognition7, indicating that LRR receptors are only indirectly involved in recognizing carbohydrate microbial factors (such as the Nod factors). Primary recognition could be performed by secreted extracellular molecules, lectins for instance, which are recognized by the LRR receptors after binding of microbial signals13.

The evolutionary relatedness of the plant and animal receptors shown in Fig. 1 is surprising if one considers that the last common ancestors of higher plants and animals separated more than 1.8 billion years ago. In animals, the relatives of the plant receptors are also involved in recognizing microbes, meaning that similar carbohydrate-recognition mechanisms could underlie the animal innate immune system. Carbohydrate recognition in the human immune system is still poorly understood, so unravelling microbe-recognition mechanisms in plants should also provide lessons for medical science.

References

  1. 1

    Stracke, S. et al. Nature 417, 959–962 (2002).

  2. 2

    Endre, G. et al. Nature 417, 962–966 (2002).

  3. 3

    Spaink, H. P., Kondorosi, A. & Hooykaas, P. J. J. The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria (Kluwer, Dordrecht, 1998).

  4. 4

    Harrison, M. J. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 361–389 (1999).

  5. 5

    Asai, T. et al. Nature 415, 977–983 (2002).

  6. 6

    Dangl, J. L. & Jones, J. D. Nature 411, 826–833 (2001).

  7. 7

    Kobe, B. & Kajava, A.V. Curr. Opin. Struct. Biol. 11, 725–732 (2001).

  8. 8

    Schuster, J. M. & Nelson, P. S. J. Leukocyte Biol. 67, 767–773 (2000).

  9. 9

    Clark, S. E. Nature Rev. Mol. Cell Biol. 2, 276–284 (2001).

  10. 10

    The Arabidopsis Genome Initiative Nature 408, 796–815 (2000).

  11. 11

    Schauser, L., Roussis, A., Stiller, J. & Stougaard, J. Nature 402, 191–195 (1999).

  12. 12

    Spaink, H. P. Nature 402, 135–136 (1999).

  13. 13

    van der Holst, P. P. G., Schlaman, H. R. M. & Spaink, H. P. Curr. Opin. Struct. Biol. 11, 608–616 (2001).

  14. 14

    Pujol, N. et al. Curr. Biol. 11, 809–821 (2001).

  15. 15

    Hajouj, T., Michelis, R. & Gepstein, S. Plant Physiol. 124, 1305–1314 (2000).

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  1. the Clusius Laboratory, Leiden University, Wassenaarseweg 64, Leiden, 2333 AL, The Netherlands

    • Herman P. Spaink

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Correspondence to Herman P. Spaink.

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