Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A receptor kinase gene regulating symbiotic nodule development


Leguminous plants are able to establish a nitrogen-fixing symbiosis with soil bacteria generally known as rhizobia. Metabolites exuded by the plant root activate the production of a rhizobial signal molecule, the Nod factor, which is essential for symbiotic nodule development1,2. This lipo-chitooligosaccharide signal is active at femtomolar concentrations, and its structure is correlated with host specificity of symbiosis3, suggesting the involvement of a cognate perception system in the plant host. Here we describe the cloning of a gene from Medicago sativa that is essential for Nod-factor perception in alfalfa, and by genetic analogy, in the related legumes Medicago truncatula and Pisum sativum. The identified ‘nodulation receptor kinase’, NORK, is predicted to function in the Nod-factor perception/transduction system (the NORK system) that initiates a signal cascade leading to nodulation. The family of ‘NORK extracellular-sequence-like’ (NSL) genes is broadly distributed in the plant kingdom, although their biological function has not been previously ascribed. We suggest that during the evolution of symbiosis an ancestral NSL system was co-opted for transduction of an external ligand, the rhizobial Nod factor, leading to development of the symbiotic root nodule.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Genetic and physical map around the Nod locus.
Figure 2: The NORK proteins.
Figure 3: Genomic hybridization with the NORK gene to different legume and non-legume plants.


  1. 1

    Lerouge, P. et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated acylated glucosamine oligosaccharide signal. Nature 344, 781–784 (1990)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Schultze, M. & Kondorosi, A. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32, 33–57 (1998)

    CAS  Article  Google Scholar 

  3. 3

    Schultze, M. & Kondorosi, A. What makes nodulation signals host-plant specific? Trends Microbiol. 3, 370–372 (1995)

    CAS  Article  Google Scholar 

  4. 4

    Peterson, M. A. & Barnes, D. K. Inheritance of ineffective nodulation and non-nodulation traits in alfalfa. Crop Sci. 21, 611–616 (1981)

    Article  Google Scholar 

  5. 5

    Dudley, M. E. & Long, S. R. A non-nodulating alfalfa mutant displays neither root hair curling nor early cell division in response to Rhizobium meliloti. Plant Cell 1, 65–72 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Ehrhardt, D. W., Wais, R. & Long, S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673–681 (1996)

    CAS  Article  Google Scholar 

  7. 7

    Felle, H. H., Kondorosi, É., Kondorosi, Á. & Schultze, M. Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J. 10, 295–301 (1996)

    CAS  Article  Google Scholar 

  8. 8

    Truchet, G. et al. Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet. 219, 65–68 (1989)

    CAS  Article  Google Scholar 

  9. 9

    Caetano-Annolés, G., Joshi, P. A. & Gresshoff, P. M. in New Horizons in Nitrogen Fixation (eds Palacios, R., Mora, J. & Newton, W. E.) 297–302 (Kluwer Academic, Dordrecht, 1993)

    Google Scholar 

  10. 10

    Bradbury, S. M., Peterson, R. L. & Bowley, S. R. Interaction between three alfalfa nodulation genotypes and two Glomus species. New Phytol. 119, 115–120 (1991)

    Article  Google Scholar 

  11. 11

    Gianinazzi-Pearson, V. Plant cell responses to arbuscular mycorrhizal fungi—getting to the roots of the symbiosis. Plant Cell 8, 1871–1883 (1996)

    Article  Google Scholar 

  12. 12

    Endre, G. et al. Genetic mapping of the non-nodulation phenotype of the mutant MN-1008 in tetraploid alfalfa (Medicago sativa). Mol. Genet. Genomics 266, 1012–1019; advance online publication, 23 January (2002) (doi:10.1007/s00438-001-0628-3)

    CAS  Article  Google Scholar 

  13. 13

    Nam, Y. W. et al. Construction of a bacterial artificial chromosome library of Medicago truncatula and identification of clones containing ethylene response genes. Theor. Appl. Genet. 98, 638–646 (1999)

    CAS  Article  Google Scholar 

  14. 14

    Kobe, B. & Deisenhofer, J. The leucine-rich repeat: a versatile binding motif. Trends Bio. Sci. 19, 415–421 (1994)

    CAS  Article  Google Scholar 

  15. 15

    Hanks, S. K. & Quinn, A. M. Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol. 200, 38–61 (1991)

    CAS  Article  Google Scholar 

  16. 16

    Schenk, P. W. & Snaar-Jagalska, B. E. Signal perception and transduction: role of protein kinases. Biochem. Biophys. Acta 1449, 1–24 (1999)

    CAS  Article  Google Scholar 

  17. 17

    Hurtley, S. M. & Helenius, A. Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277–307 (1989)

    CAS  Article  Google Scholar 

  18. 18

    Catoira, R. et al. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12, 1647–1665 (2000)

    CAS  Article  Google Scholar 

  19. 19

    Schneider, A. et al. Genetic mapping and functional analysis of a nodulation-defective mutant (sym19) of pea (Pisum sativum L.). Mol. Gen. Genet. 262, 1–11 (1999)

    CAS  Article  Google Scholar 

  20. 20

    Boisson-Dernier, A. et al. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol. Plant-Microbe Interact. 14, 695–700 (2001)

    CAS  Article  Google Scholar 

  21. 21

    Doyle, J. J. Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci. 3, 473–478 (1998)

    Article  Google Scholar 

  22. 22

    Shiu, S.-H. & Bleecker, A. B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl Acad. Sci. USA 98, 10763–10768 (2001)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Hajouj, T., Michelis, R. & Gepstein, S. Cloning and characterization of a receptor-like protein kinase gene associated with senescence. Plant Physiol. 124, 1305–1314 (2000)

    CAS  Article  Google Scholar 

  24. 24

    Deeken, R. & Kaldenhoff, R. Light-repressible receptor protein kinase: a novel photo-regulated gene from Arabidopsis thaliana. Planta 202, 479–486 (1997)

    CAS  Article  Google Scholar 

  25. 25

    Pingret, J. L., Journet, E. P. & Barker, D. G. Rhizobium Nod factor signalling. Evidence for a G protein-mediated transduction mechanism. Plant Cell 10, 659–672 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Wais, R. J. et al. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl Acad. Sci. USA 97, 13407–13412 (2000)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Stougaard, J. Genetics and genomics of root symbiosis. Curr. Opin. Plant Biol. 4, 328–335 (2001)

    CAS  Article  Google Scholar 

  28. 28

    Walker, S. A. et al. Dissection of nodulation signalling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc. Natl Acad. Sci. USA 97, 13413–13418 (2000)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Szabados, L., Charrier, B., Kondorosi, A., Debruijn, F. J. & Ratet, P. New plant promoter and enhancer testing vectors. Mol. Breeding 1, 419–423 (1995)

    CAS  Article  Google Scholar 

  30. 30

    Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673–4680 (1994)

    CAS  Article  Google Scholar 

Download references


We thank D. Cook for comments, suggestions and help in finalizing the manuscript, A. Kondorosi for critical reading of the manuscript, A. Perhald for help in transformation experiments, and P. Kiss, S. Jenei, K. Lehoczky, Z. Liptay, P. Somkúti and A. Lengyel for technical assistance. This work was supported by the BRC, Szeged, Hungary, the Bástyai-Holczer Foundation, the Hungarian Academy of Sciences, the Hungarian Scientific Research Fund, the Hungarian National Committee for Technical Development, the Szechenyi Fund of the Hungarian Ministry of Education, the EuDicotMap and the Medicago projects of the European Union.

Author information



Corresponding author

Correspondence to György B. Kiss.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Endre, G., Kereszt, A., Kevei, Z. et al. A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966 (2002).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing