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. 1995 Aug;108(4):1607–1614. doi: 10.1104/pp.108.4.1607

Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa.

C Staehelin 1, M Schultze 1, E Kondorosi 1, A Kondorosi 1
PMCID: PMC157541  PMID: 12228566

Abstract

Extracellular enzymes from alfalfa (Medicago sativa L.) involved in the degradation of nodulation (Nod) factors could be distinguished by their different cleavage specificities and were separated by lectin affinity chromatography. A particular glycoprotein was able to release an acylated lipo-disaccharide from all tested Nod factors having an oligosaccharide chain length of four or five residues. Structural modifications of the basic lipo-chitooligosaccharide did not affect the cleavage site and had only weak influence on the cleavage efficiency of Nod factors tested. The acylated lipo-trisaccharide was resistant to degradation. When alfalfa roots were preincubated with Nod factors at nanomolar concentrations, the activity of the dimer-forming enzyme was stimulated up to 6-fold within a few hours. The inducing activity of Nod factors decreased in the order NodRm-IV(C16:2,Ac,S) > NodRm-IV(C16:2,S) and NodRm-V(C16:2,Ac,S) > NodRm-V(C16:2,S) > NodRm-IV(C16:0,S) > NodRm-IV(C16:2). Pretreatment with NodRm-III(C16:2) as well as unmodified chitooligosaccharides did not stimulate the dimer-forming enzyme. Roots preincubated with Rhizobium meliloti showed similar stimulation of the dimer-forming activity. Mutant strains unable to produce Nod factors did not enhance the hydrolytic activity. These results indicate a rapid feedback inactivation of Nod signals after their perception by the host plant alfalfa.

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Selected References

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  1. Bauer P., Crespi M. D., Szécsi J., Allison L. A., Schultze M., Ratet P., Kondorosi E., Kondorosi A. Alfalfa Enod12 genes are differentially regulated during nodule development by Nod factors and Rhizobium invasion. Plant Physiol. 1994 Jun;105(2):585–592. doi: 10.1104/pp.105.2.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bloemberg G. V., Thomas-Oates J. E., Lugtenberg B. J., Spaink H. P. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol Microbiol. 1994 Feb;11(4):793–804. doi: 10.1111/j.1365-2958.1994.tb00357.x. [DOI] [PubMed] [Google Scholar]
  3. Caetano-Anollés G., Gresshoff P. M. Plant genetic control of nodulation. Annu Rev Microbiol. 1991;45:345–382. doi: 10.1146/annurev.mi.45.100191.002021. [DOI] [PubMed] [Google Scholar]
  4. Carlson R. W., Price N. P., Stacey G. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):684–695. doi: 10.1094/mpmi-7-0684. [DOI] [PubMed] [Google Scholar]
  5. Collinge D. B., Kragh K. M., Mikkelsen J. D., Nielsen K. K., Rasmussen U., Vad K. Plant chitinases. Plant J. 1993 Jan;3(1):31–40. doi: 10.1046/j.1365-313x.1993.t01-1-00999.x. [DOI] [PubMed] [Google Scholar]
  6. Crespi M. D., Jurkevitch E., Poiret M., d'Aubenton-Carafa Y., Petrovics G., Kondorosi E., Kondorosi A. enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J. 1994 Nov 1;13(21):5099–5112. doi: 10.1002/j.1460-2075.1994.tb06839.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Demont N., Debellé F., Aurelle H., Dénarié J., Promé J. C. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem. 1993 Sep 25;268(27):20134–20142. [PubMed] [Google Scholar]
  9. Dénarié J., Cullimore J. Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell. 1993 Sep 24;74(6):951–954. doi: 10.1016/0092-8674(93)90717-5. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Flach J., Pilet P. E., Jollès P. What's new in chitinase research? Experientia. 1992 Aug 15;48(8):701–716. doi: 10.1007/BF02124285. [DOI] [PubMed] [Google Scholar]
  12. Heidstra R., Geurts R., Franssen H., Spaink H. P., Van Kammen A., Bisseling T. Root Hair Deformation Activity of Nodulation Factors and Their Fate on Vicia sativa. Plant Physiol. 1994 Jul;105(3):787–797. doi: 10.1104/pp.105.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Journet E. P., Pichon M., Dedieu A., de Billy F., Truchet G., Barker D. G. Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J. 1994 Aug;6(2):241–249. doi: 10.1046/j.1365-313x.1994.6020241.x. [DOI] [PubMed] [Google Scholar]
  14. Kondorosi E., Gyuris J., Schmidt J., John M., Duda E., Hoffmann B., Schell J., Kondorosi A. Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation. EMBO J. 1989 May;8(5):1331–1340. doi: 10.1002/j.1460-2075.1989.tb03513.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Roby D., Gadelle A., Toppan A. Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochem Biophys Res Commun. 1987 Mar 30;143(3):885–892. doi: 10.1016/0006-291x(87)90332-9. [DOI] [PubMed] [Google Scholar]
  17. Savouré A., Magyar Z., Pierre M., Brown S., Schultze M., Dudits D., Kondorosi A., Kondorosi E. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J. 1994 Mar 1;13(5):1093–1102. doi: 10.1002/j.1460-2075.1994.tb06358.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Stintzi A., Heitz T., Prasad V., Wiedemann-Merdinoglu S., Kauffmann S., Geoffroy P., Legrand M., Fritig B. Plant 'pathogenesis-related' proteins and their role in defense against pathogens. Biochimie. 1993;75(8):687–706. doi: 10.1016/0300-9084(93)90100-7. [DOI] [PubMed] [Google Scholar]
  19. Yang W. C., de Blank C., Meskiene I., Hirt H., Bakker J., van Kammen A., Franssen H., Bisseling T. Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell. 1994 Oct;6(10):1415–1426. doi: 10.1105/tpc.6.10.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]

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