Skip to main content

Thank you for visiting nature.com. 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.

  • Letter
  • Published:

A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals

Abstract

Plants belonging to the legume family develop nitrogen-fixing root nodules in symbiosis with bacteria commonly known as rhizobia. The legume host encodes all of the functions necessary to build the specialized symbiotic organ, the nodule, but the process is elicited by the bacteria1,2,3. Molecular communication initiates the interaction, and signals, usually flavones, secreted by the legume root induce the bacteria to produce a lipochitin-oligosaccharide signal molecule (Nod-factor), which in turn triggers the plant organogenic process4,5,6,7. An important determinant of bacterial host specificity is the structure of the Nod-factor, suggesting that a plant receptor is involved in signal perception and signal transduction initiating the plant developmental response8,9. Here we describe the cloning of a putative Nod-factor receptor kinase gene (NFR5) from Lotus japonicus. NFR5 is essential for Nod-factor perception and encodes an unusual transmembrane serine/threonine receptor-like kinase required for the earliest detectable plant responses to bacteria and Nod-factor. The extracellular domain of the putative receptor has three modules with similarity to LysM domains known from peptidoglycan-binding proteins and chitinases. Together with an atypical kinase domain structure this characterizes an unusual receptor-like kinase.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Map-based cloning of NFR5.
Figure 2: Structure and domains of the NFR5 protein.
Figure 3: Expression of Lotus NFR5 and pea SYM10.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  2. Truchet, G. et al. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670–673 (1991)

    Article  ADS  CAS  Google Scholar 

  3. Spaink, H. P. et al. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–130 (1991)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Lopez-Lara, I. M. et al. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol. Microbiol. 15, 627–638 (1995)

    Article  CAS  Google Scholar 

  6. Niwa, S. et al. Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol. Plant Microbe Interact. 14, 848–856 (2001)

    Article  CAS  Google Scholar 

  7. Long, S. R. Rhizobium symbiosis: nod factors in perspective. Plant Cell 8, 1885–1898 (1996)

    Article  CAS  Google Scholar 

  8. Ardourel, M. et al. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6, 1357–1374 (1994)

    Article  CAS  Google Scholar 

  9. Pacios-Bras, C. et al. A Lotus japonicus nodulation system based on heterologous expression of the fucosyl transferase NodZ and the acetyl transferase NolL in Rhizobium leguminosarum. Mol. Plant Microbe Interact. 13, 475–479 (2000)

    Article  CAS  Google Scholar 

  10. Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592 (2003)

    Article  ADS  CAS  Google Scholar 

  11. Wegel, E., Schauser, L., Sandal, N., Stougaard, J. & Parniske, M. Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol. Plant Microbe Interact. 11, 933–936 (1998)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Sandal, N. et al. A genetic linkage map of the model legume Lotus japonicus and strategies for fast mapping of new loci. Genetics 161, 1673–1683 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Nakamura, Y. et al. Structural analysis of a Lotus japonicus genome. II. Sequence features and mapping of sixty-five TAC clones which cover the 6.5-Mb regions of the genome. DNA Res. 9, 63–70 (2002)

    Article  CAS  Google Scholar 

  15. Steen, A. et al. Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 278, 23874–23881 (2003)

    Article  CAS  Google Scholar 

  16. Butler, A. R., O'Donnell, R. W., Martin, V. J., Gooday, G. W. & Stark, M. J. Kluyveromyces lactis toxin has an essential chitinase activity. Eur. J. Biochem. 199, 483–488 (1991)

    Article  CAS  Google Scholar 

  17. Amon, P., Haas, E. & Sumper, M. The sex-inducing pheromone and wounding trigger the same set of genes in the multicellular green alga Volvox. Plant Cell 10, 781–789 (1998)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Huse, M. & Kuriyan, J. The conformational plasticity of protein kinases. Cell 109, 275–282 (2002)

    Article  CAS  Google Scholar 

  20. Duc, G. & Messager, A. Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Sci. 60, 207–213 (1989)

    Article  Google Scholar 

  21. Kneen, B. E., Weeden, N. F. & LaRue, T. A. Non-nodulating mutants of Pisum sativum (L.) cv. Sparkle. J. Hered. 85, 129–132 (1994)

    Article  Google Scholar 

  22. Schneider, A. et al. Mapping of the nodulation loci sym9 and sym10 of pea (Pisum sativumL). Theor. Appl. Genet. 104, 1312–1316 (2002)

    Article  CAS  Google Scholar 

  23. Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962 (2002)

    Article  ADS  CAS  Google Scholar 

  24. Engvild, K. C. Nodulation and nitrogen fixation mutants of pea, Pisum sativum. Theor. Appl. Genet. 74, 711–713 (1987)

    Article  CAS  Google Scholar 

  25. Wikstrom, N., Savolainen, V. & Chase, M. W. Evolution of the angiosperms: calibrating the family tree. Proc. R. Soc. Lond. B 268, 2211–2220 (2001)

    Article  CAS  Google Scholar 

  26. Bateman, A. & Bycroft, M. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299, 1113–1119 (2000)

    Article  CAS  Google Scholar 

  27. Schauser, L. et al. Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol. Gen. Genet. 259, 414–423 (1998)

    Article  CAS  Google Scholar 

  28. Szczyglowski, K. et al. Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 11, 684–697 (1998)

    Article  CAS  Google Scholar 

  29. Handberg, K. & Stougaard, J. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J. 2, 487–496 (1992)

    Article  Google Scholar 

  30. Stougaard, J. Agrobacterium rhizogenes as a vector for transforming higher plants. Methods Mol. Biol. 49, 49–61 (1995)

    CAS  PubMed  Google Scholar 

  31. Krusell, L. et al. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422–426 (2002)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Ambrose, A. Downie and K. Engvild for providing seeds from plants with sym10 alleles. S.R. was supported by an EU Marie Curie Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jens Stougaard.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

41586_2003_BFnature02045_MOESM1_ESM.doc

Supplementary Information: Alignment of NFR5 and the orthologous SYM10 protein with the most similar proteins from Medicago truncatula (Acc Ac126779) and rice (Acc Ac103891). Black boxes indicate amino acid conserved in all four proteins and grey boxes amino acids conserved in three of the proteins. (DOC 32 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Madsen, E., Madsen, L., Radutoiu, S. et al. A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals. Nature 425, 637–640 (2003). https://doi.org/10.1038/nature02045

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02045

This article is cited by

Comments

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.

Search

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