Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1995 Aug;108(4):1587–1595. doi: 10.1104/pp.108.4.1587

Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja.

T J Stokkermans 1, S Ikeshita 1, J Cohn 1, R W Carlson 1, G Stacey 1, T Ogawa 1, N K Peters 1
PMCID: PMC157539  PMID: 7659753

Abstract

Rhizobia synthesize a class of lipo-chitin oligosaccharides that induce root hair deformation and induce the initiation of nodule structures on legume roots. These lipo-chitin oligosaccharides are tetra- and penta-lipo-oligosaccharides of N-acetylglucosamine with an acyl substitution on the nonreducing end and are commonly known as Nod factors. In this study, we demonstrate that synthetic analogs of natural product Nod factors have the same biological activities. To determine structure-activity relationships, a collection of synthetic and natural product lipo-chitin oligosaccharides was assayed on Glycine soja. All biologically active lipo-chitin oligosaccharides induced both root hair deformation and nodule initiations on G. soja. The most active lipo-chitin oligosaccharides deformed root hairs at 10(-15) M and induced nodules at 1 ng of lipo-chitin oligosaccharide per spot inoculation. Plant responses demonstrate an interdependence of backbone length and the presence of substitutions on the reducing end. Lipo-chitin oligosaccharides containing four N-acetylglucosamine residues were active only without a reducing end modification, whereas lipo-chitin oligosaccharides containing five N-acetylglucosamine residues were active only with reducing end modification. The plant thus recognizes lipo-chitin oligosaccharides without reducing end substitutions despite the importance of these modifications for host range.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Augur C., Yu L., Sakai K., Ogawa T., Sinaÿ P., Darvill A. G., Albersheim P. Further studies of the ability of xyloglucan oligosaccharides to inhibit auxin-stimulated growth. Plant Physiol. 1992 May;99(1):180–185. doi: 10.1104/pp.99.1.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bono J. J., Riond J., Nicolaou K. C., Bockovich N. J., Estevez V. A., Cullimore J. V., Ranjeva R. Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J. 1995 Feb;7(2):253–260. doi: 10.1046/j.1365-313x.1995.7020253.x. [DOI] [PubMed] [Google Scholar]
  3. Carlson R. W., Sanjuan J., Bhat U. R., Glushka J., Spaink H. P., Wijfjes A. H., van Brussel A. A., Stokkermans T. J., Peters N. K., Stacey G. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and II strains of Bradyrhizobium japonicum. J Biol Chem. 1993 Aug 25;268(24):18372–18381. [PubMed] [Google Scholar]
  4. Cheong J. J., Alba R., Côté F., Enkerli J., Hahn M. G. Solubilization of functional plasma membrane-localized hepta-beta-glucoside elicitor-binding proteins from soybean. Plant Physiol. 1993 Dec;103(4):1173–1182. doi: 10.1104/pp.103.4.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheong J. J., Birberg W., Fügedi P., Pilotti A., Garegg P. J., Hong N., Ogawa T., Hahn M. G. Structure-activity relationships of oligo-beta-glucoside elicitors of phytoalexin accumulation in soybean. Plant Cell. 1991 Feb;3(2):127–136. doi: 10.1105/tpc.3.2.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. De Jong A. J., Heidstra R., Spaink H. P., Hartog M. V., Meijer E. A., Hendriks T., Schiavo F. L., Terzi M., Bisseling T., Van Kammen A. Rhizobium Lipooligosaccharides Rescue a Carrot Somatic Embryo Mutant. Plant Cell. 1993 Jun;5(6):615–620. doi: 10.1105/tpc.5.6.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ehrhardt D. W., Atkinson E. M., Long S. R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science. 1992 May 15;256(5059):998–1000. doi: 10.1126/science.10744524. [DOI] [PubMed] [Google Scholar]
  8. Franssen H. J., Vijn I., Yang W. C., Bisseling T. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol. 1992 May;19(1):89–107. doi: 10.1007/BF00015608. [DOI] [PubMed] [Google Scholar]
  9. Hartwig U. A., Maxwell C. A., Joseph C. M., Phillips D. A. Chrysoeriol and Luteolin Released from Alfalfa Seeds Induce nod Genes in Rhizobium meliloti. Plant Physiol. 1990 Jan;92(1):116–122. doi: 10.1104/pp.92.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J. C., Dénarié J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990 Apr 19;344(6268):781–784. doi: 10.1038/344781a0. [DOI] [PubMed] [Google Scholar]
  11. Luka S., Sanjuan J., Carlson R. W., Stacey G. nolMNO genes of Bradyrhizobium japonicum are co-transcribed with nodYABCSUIJ, and nolO is involved in the synthesis of the lipo-oligosaccharide nodulation signals. J Biol Chem. 1993 Dec 25;268(36):27053–27059. [PubMed] [Google Scholar]
  12. Maxwell C. A., Hartwig U. A., Joseph C. M., Phillips D. A. A Chalcone and Two Related Flavonoids Released from Alfalfa Roots Induce nod Genes of Rhizobium meliloti. Plant Physiol. 1989 Nov;91(3):842–847. doi: 10.1104/pp.91.3.842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McDougall G. J., Fry S. C. Structure-activity relationships for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol. 1989 Mar;89(3):883–887. doi: 10.1104/pp.89.3.883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mergaert P., Van Montagu M., Promé J. C., Holsters M. Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1551–1555. doi: 10.1073/pnas.90.4.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nakahara Y., Ogawa T. Stereoselective total synthesis of dodecagalacturonic acid, a phytoalexin elicitor of soybean. Carbohydr Res. 1990 Sep 19;205:147–159. doi: 10.1016/0008-6215(90)80135-p. [DOI] [PubMed] [Google Scholar]
  16. Nakahara Y., Ogawa T. Synthesis of (1----4)-linked galacturonic acid trisaccharides, a proposed plant wound-hormone and a stereoisomer. Carbohydr Res. 1990 Apr 25;200:363–375. doi: 10.1016/0008-6215(90)84203-7. [DOI] [PubMed] [Google Scholar]
  17. Nieuwkoop A. J., Banfalvi Z., Deshmane N., Gerhold D., Schell M. G., Sirotkin K. M., Stacey G. A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. J Bacteriol. 1987 Jun;169(6):2631–2638. doi: 10.1128/jb.169.6.2631-2638.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Peters N. K., Frost J. W., Long S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science. 1986 Aug 29;233(4767):977–980. doi: 10.1126/science.3738520. [DOI] [PubMed] [Google Scholar]
  19. Poupot R., Martinez-Romero E., Promé J. C. Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus. Biochemistry. 1993 Oct 5;32(39):10430–10435. doi: 10.1021/bi00090a019. [DOI] [PubMed] [Google Scholar]
  20. Price N. P., Relić B., Talmont F., Lewin A., Promé D., Pueppke S. G., Maillet F., Dénarié J., Promé J. C., Broughton W. J. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol Microbiol. 1992 Dec;6(23):3575–3584. doi: 10.1111/j.1365-2958.1992.tb01793.x. [DOI] [PubMed] [Google Scholar]
  21. Roche P., Debellé F., Lerouge P., Vasse J., Truchet G., Promé J. C., Dénarié J. The lipo-oligosaccharidic symbiotic signals of Rhizobium meliloti. Biochem Soc Trans. 1992 May;20(2):288–291. doi: 10.1042/bst0200288. [DOI] [PubMed] [Google Scholar]
  22. Sanjuan J., Carlson R. W., Spaink H. P., Bhat U. R., Barbour W. M., Glushka J., Stacey G. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8789–8793. doi: 10.1073/pnas.89.18.8789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shibuya N., Kaku H., Kuchitsu K., Maliarik M. J. Identification of a novel high-affinity binding site for N-acetylchitooligosaccharide elicitor in the membrane fraction from suspension-cultured rice cells. FEBS Lett. 1993 Aug 23;329(1-2):75–78. doi: 10.1016/0014-5793(93)80197-3. [DOI] [PubMed] [Google Scholar]
  24. Spaink H. P., Sheeley D. M., van Brussel A. A., Glushka J., York W. S., Tak T., Geiger O., Kennedy E. P., Reinhold V. N., Lugtenberg B. J. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature. 1991 Nov 14;354(6349):125–130. doi: 10.1038/354125a0. [DOI] [PubMed] [Google Scholar]
  25. Stacey G., Luka S., Sanjuan J., Banfalvi Z., Nieuwkoop A. J., Chun J. Y., Forsberg L. S., Carlson R. nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J Bacteriol. 1994 Feb;176(3):620–633. doi: 10.1128/jb.176.3.620-633.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Staehelin C., Granado J., Müller J., Wiemken A., Mellor R. B., Felix G., Regenass M., Broughton W. J., Boller T. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2196–2200. doi: 10.1073/pnas.91.6.2196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stokkermans T. J., Peters N. K. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta. 1994;193(3):413–420. doi: 10.1007/BF00201821. [DOI] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES