Advertisement

Role of rhizobial lipo-chitin oligosaccharide signal molecules in root nodule organogenesis

  • Herman P. Spaink
  • Ben J. J. Lugtenberg

Abstract

The role of oligosaccharide molecules in plant development is discussed. In particular the role of the rhizobial lipo-chitin oligosaccharide (LCO) signal molecules in the development of the root nodule indicates that oligosaccharides play an important role in organogenesis in plants. Recent results of the analyses of structures and of the biosynthesis of the LCO molecules are summarized in this paper. The knowledge and technologies that resulted from these studies will be important tools for further studying the function of LCO signals in the plant and in the search for analogous signal molecules produced by plants.

Key words

plant-microbe interactions nod metabolites nod genes oligosaccharins 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Aldington S, Fry SC: Oligosaccharins. Adv Bot Res 19: 1–101 (1993).CrossRefGoogle Scholar
  2. 2.
    Atkinson EM, Ehrhardt DW, Long SR: In vitro activity of the nodH gene product from Rhizobium meliloti. In: Sixth International Symposium on Molecular PlantMicrobe Interactions, Program and Abstracts, abstract 45. University of Washington, Seattle, WA (1992).Google Scholar
  3. 3.
    Atkinson EM, Long SR: Homology of Rhizobium meliloti NodC to polysaccharide polymerizing enzymes. Mol Plant-Microbe Interact 5: 439–442 (1992).PubMedCrossRefGoogle Scholar
  4. 4.
    Ayers AR, Ebel J, Finelli F, Berger N, Albersheim P: Host-pathogen interactions. IX. Quantitative assays of elicitor activity and characterization of the elicitor present in the extracellular medium of cultures of Phytophthora megasperma var. sojae. Plant Physiol 57: 751–759 (1976).PubMedCrossRefGoogle Scholar
  5. 5.
    Baev N, Endre G, Petrovics G, Banfalvi Z, Kondorosi A: Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Mol Gen Genet 228: 113–124(1991).PubMedCrossRefGoogle Scholar
  6. 6.
    Bakhuizen R: The plant cytoskeleton in the Rhizobium- legume symbiosis. Ph.D. thesis, Leiden University, Netherlands (1988).Google Scholar
  7. 7.
    Barber MS, Bertram RE, Ride JP: Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Path 34: 3–12 (1989).CrossRefGoogle Scholar
  8. 8.
    Bec-Ferte MP, Savagnac A, Pueppke SG, Prome JC: Nod factors from Rhizobium fredii USDA257. In: Palacios R, Mora J, Newton WE (eds) New Horizons in Nitrogen Fixation, pp. 157–158. Kluwer Academic Publishers, Dordrecht (1993).Google Scholar
  9. 9.
    Benhamou N, Asselin A: Attempted localization of a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls. Biol Cell 67: 341–350 (1989).Google Scholar
  10. 10.
    Bloemberg GV, Thomas-Oates JE, Lugtenberg BJJ, Spaink HP: Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol Microbiol 11: 793–804(1994).PubMedCrossRefGoogle Scholar
  11. 11.
    Bowles DJ: Defense-related proteins in higher plants. Ann Rev Biochem 59:873–907 (1990).PubMedCrossRefGoogle Scholar
  12. 12.
    Bulawa CE, Wasco W: Chitin and nodulation. Nature 353: 710 (1991).PubMedCrossRefGoogle Scholar
  13. 13.
    Bulawa CE: CSD2,CSD3 and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol Cell Biol 12: 1764–1776 (1992).PubMedGoogle Scholar
  14. 14.
    Bulawa CE: Genetics and molecular biology of chitin synthesis in fungi. Annu Rev Microbiol 47: 505–534 (1993).PubMedCrossRefGoogle Scholar
  15. 15.
    Carlson RW, Sanjuan J, Bhat R, Glushka J, Spaink HP, Wijfjes HM, van Brussel AN, Stokkermans TJW, Peters K, Stacey G: The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and type II strains of Bradyrhizobium japonicum. J Biol Chem 268: 18372–18381 (1993).PubMedGoogle Scholar
  16. 16.
    Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K: Plant chitinases. Plant J 3: 31–40 (1993).PubMedCrossRefGoogle Scholar
  17. 17.
    Davis KR, Darvill AG, Albersheim P, Dell A: Hostpathogen interactions. XXIX. Oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexins in soybean. Plant Physiol 80: 568–577 (1986).PubMedCrossRefGoogle Scholar
  18. 18.
    Debelle F, Rosenberg C, Dénarié J: The Rhizobium, Bradyrhizobium and Azorhizobium NodC proteins are homologous to yeast chitin synthases. Mol Plant-Microbe Interact 3: 317–326(1992).Google Scholar
  19. 19.
    de Jong AJ, Cordewener J, Lo Schiavo F, Terzi M, Vandekerckhove J, Van Kammen A, de Vries S: A car- rot somatic embryo mutant is rescued by chitinase. Plant Cell 4: 425–433 (1992).PubMedGoogle Scholar
  20. 20.
    de Jong AJ, Heidstra R, Spaink HP, Hartog MV, Hendriks T, Lo Schiavo F, Terzi M, Bisseling T, Van Kammen A, de Vries S: A plant somatic embryo mutant is rescued by rhizobial lipo-oligosaccharides. Plant Cell 5: 615–620 (1993).PubMedGoogle Scholar
  21. 21.
    Demont N, Debellé F, Aurelle H, Dénarié J, Promé JC: Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem 268: 20134–20142 (1993).PubMedGoogle Scholar
  22. 22.
    Dénarié J, Cullimore J: Lipo-oligosaccharide nodulation factors: a new class of signalling molecules mediating recognition and morphogenesis. Cell 74: 951–954 (1993).PubMedCrossRefGoogle Scholar
  23. 23.
    Deverall BJ, Deakin AL: Genetic tests of the basis of wheat cultivar selectivity in symptom elicitation by preparations from rust pathogens. Physiol Mol Plant Path 30: 225–232 (1987).CrossRefGoogle Scholar
  24. 24.
    Ehrhardt DW, Atkinson EM, Long SR: Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998–1000 (1992).PubMedCrossRefGoogle Scholar
  25. 25.
    Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA: Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol Microbiol 10: 351–360 (1993).PubMedCrossRefGoogle Scholar
  26. 26.
    Fisher RF, Long SR: Rhizobium-plant signal exchange. Nature 357: 655–660 (1992).PubMedCrossRefGoogle Scholar
  27. 27.
    Fry SC, Aldington S, Hetherington PR, Aitken J: Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol 103: 1–5 (1993).PubMedCrossRefGoogle Scholar
  28. 28.
    Geelen D, Mergaert P, Geremia RA, Goormachtig S, Van Montagu M, Holsters M: Identification of nodSUIJ genes in locus 1 of Azorhizobium caulinodans: evidence that nodS encodes a methyltransferase involved in Nod factor modification. Mol Microbiol 9: 145–154 (1993).PubMedCrossRefGoogle Scholar
  29. 29.
    Geiger O, Spaink HP, Kennedy EP: Isolation of Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4’-phosphopantetheine prosthetic group. J Bact 173: 2872–2878 (1991).PubMedGoogle Scholar
  30. 30.
    Heidstra R, Geurts R, Franssen H, Spaink HP, Van Kammen A, Bisseling T: A semi-quantitative root hair deformation assay to study the activity and fate of Nod factors. Plant Physiol 105: 787–797 (1994).PubMedGoogle Scholar
  31. 31.
    Horvath B, Heidstra R, Lados M, Moerman M, Spaink HP, Promé J-C, Van Kammen A, Bisseling T: Induction of pea early nodulin expression by Nod factors of Rhizobium. Plant J 4: 727–733 (1993).PubMedCrossRefGoogle Scholar
  32. 32.
    John M, Röhrig H, Schmidt J, Wieneke U, Schell J: Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci USA 90: 625–629 (1993).PubMedCrossRefGoogle Scholar
  33. 33.
    Kafetzopoulos D, Thireos G, Vournakis JN, Bouriotis V: The primary structure of a fungal chitin deacetylase reveals the function for two bacterial gene products Proc Natl Acad Sci USA 90: 8005–8008 (1993).PubMedCrossRefGoogle Scholar
  34. 34.
    Kouchi H, Hata S: Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238: 106–119(1993).PubMedGoogle Scholar
  35. 35.
    Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J: Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–784 (1990).PubMedCrossRefGoogle Scholar
  36. 36.
    Libbenga KR, Van Iren F, Bogers RJ, Schraag-Lamers MF: The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114: 19–39 (1973).Google Scholar
  37. 37.
    Marie C, Barny M-A, Downie JA: Rhizobium leguminosarum has two glucosamine synthases, GlmS and NodM, required for nodulation and development of nitrogen fixing nodules. Mol Microbiol 6: 843–851 (1992).PubMedCrossRefGoogle Scholar
  38. 38.
    Mergaert P, Van Montagu M, Promé J-C, Holsters M: Three unusual modifications, a D-arabinosyl, a N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc Natl Acad Sci USA 90: 1551–1555 (1993).PubMedCrossRefGoogle Scholar
  39. 39.
    Mohnen D, Eberhard S, Marfa V, Doubrava N, Toubart P, Gollin DJ, Gruber TA, Nuri W, Albersheim P, Darvill AG: The control of root, vegetative shoot and flower morphogenesis in tobacco thin cell-layer explants (TCLs). Development 108: 191–201 (1990).PubMedGoogle Scholar
  40. 40.
    Pichon M, Journet EP, Dedieu A, de Billy F, Truchet G, Barker DG: Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 40: 1199– 1211 (1992).Google Scholar
  41. 41.
    Poupot R, Martinez-Romero E, Prome J-C: Nodulation factors from Rhizobium tropici are sulphated or nonsulphated chitopentasaccharides containing an N-methyl- N-acylglucosaminyl terminus. Biochemistry 32: 10430–10435 (1993).PubMedCrossRefGoogle Scholar
  42. 42.
    Price NPJ, Relic B, Talmont F, Lewin A, Prome D, Pueppke SG, Maillet F, Denarie J, Prome J-C, Broughton WJ: Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated Mol Microbiol 6: 3575–3584 (1992).PubMedCrossRefGoogle Scholar
  43. 43.
    Recourt K: Flavonoids in the early Rhizobium-legume interaction. Ph.D. thesis, Leiden University, Netherlands (1991).Google Scholar
  44. 44.
    Recourt K, Schripsema J, Kijne JW, Van Brussel AAN, Lugtenberg BJJ: Inoculation of Vicia sativa subsp. nigra roots with R. leguminosarum biovar. viciae results in release of nod gene activating flavanones and chalcones. Plant Mol Biol 16: 841–852 (1991).PubMedCrossRefGoogle Scholar
  45. 45.
    Relic B, Talmont F, Kopcinska J, Golinowski W, Promé J-C, Broughton WJ: Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant-Microbe Interact 6: 764–774 (1993).PubMedCrossRefGoogle Scholar
  46. 46.
    Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, Truchet G, Dénarié J, Promé JC: Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulphation of lipo-oligosaccharide signals. Cell 67: 1131–1143 (1991).PubMedCrossRefGoogle Scholar
  47. 47.
    Rosa F, Sargent TD, Rebbert ML, Michaels GS, Jamrich M, Grunz H, Jonas E, Winkles J A, Dawid IB: Accumulation and decay of DG42 gene products follow a gradient pattern during Xenopus embryogenesis. Devel Biol 129: 114–123 (1988).CrossRefGoogle Scholar
  48. 48.
    Ryan CA: Oligosaccharide signals: From plant defense to parasite offense. Proc Natl Acad Sci USA 91: 1–2 (1994).PubMedCrossRefGoogle Scholar
  49. 49.
    Sandal NN, Marcker KA: Some nodulin and Nod proteins show similarity to specific animal proteins. In: Gresshoff PM, Roth LE, Stacey G, Newton WE (eds) Nitrogen Fixation: Achievements and Objectives, pp. 687–692. Chapman and Hall, New York (1990).Google Scholar
  50. 50.
    Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, Glushka J, Stacey G: A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci USA 89: 8789–8793 (1992).PubMedCrossRefGoogle Scholar
  51. 51.
    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 inMedicago microcallus suspensions. EMBO J 13: 1093–1102(1994).Google Scholar
  52. 52.
    Scheres B, Van de Wiel C, Zalensky A, Horvath B, Spaink HP, Van Eck H, Zwartkruis F, Wolters A-M, Gloudemans T, Van Kammen A, Bisseling T: The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell 60: 281–294 (1990).PubMedCrossRefGoogle Scholar
  53. 53.
    Schmidt J, Röhrig H, John M, Wieneke U, Stacey G, Koncz C, Schell J: Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J 4: 651–658 (1993).CrossRefGoogle Scholar
  54. 54.
    Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka JN, Endre G, Géro SD, Kondorosi A: Rhizobium meliloti produces a family of sulphated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89: 192–196 (1992).PubMedCrossRefGoogle Scholar
  55. 55.
    Schwedock J, Long SR: ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348: 644–647 (1990).PubMedCrossRefGoogle Scholar
  56. 56.
    Schwedock J, Long SR: Rhizobium meliloti genes involved in sulphate activation: The two copies of nodPQ and a new locus saa. Genetics 132: 899–909 (1992).PubMedGoogle Scholar
  57. 57.
    Sharp JK, McNeil M, Albersheim P: The primary structures of one elicitor-active and seven elicitor-inactive hexa(β-D-glucopyranosyl)-D-glucitols isolated from the mycelian walls of Phytophthora megasperma f.sp. glycinea. J Biol Chem 259: 11321–11336 (1984).PubMedGoogle Scholar
  58. 58.
    Shearman CA, Rossen L, Johnston AWB, Downie J A: The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO J 5: 647–652 (1986).PubMedGoogle Scholar
  59. 59.
    Smit G, Lugtenberg BJJ, Kijne JW: Isolation of nodulation factor from the stele of the roots of Pisum sativum. In: Halick RB (ed) Molecular Biology of Plant Cell Growth and Development, Program and Abstracts, abstract 1427. Department of Biochemistry, Tucson, AR (1991).Google Scholar
  60. 60.
    Spaink HP, Sheeley DM, Van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJJ: A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125–130 (1991).PubMedCrossRefGoogle Scholar
  61. 61.
    Spaink HP: Rhizobial lipo-oligosaccharides: answers and questions. Plant Mol Biol 20: 977–986 (1992).PubMedCrossRefGoogle Scholar
  62. 62.
    Spaink HP, Wijfjes AHM, Van Vliet, TB, Kijne JW, Lugtenberg BJJ: Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis: are analogous lipophilic chitin derivatives produced by the plant? Aust J Plant Physiol 20: 381–392 (1993).CrossRefGoogle Scholar
  63. 63.
    Spaink HP, Wijfjes AHM, Van der Drift KMGM, Haverkamp J, Thomas-Oates JE, Lugtenberg BJJ: Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol Microbiol 13: 821–831 (1994).PubMedCrossRefGoogle Scholar
  64. 64.
    Staehelin C, Granado J, Müller J, Wiemken A, Mellor RB, Felix G, Regenass M, Broughton WJ, Boiler T: Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci USA 91: 2196–2200 (1994).PubMedCrossRefGoogle Scholar
  65. 65.
    Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, Chun JY, Forsberg LS, Carlson R: nodZ, a unique hostspecific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobgium japonicum. J Bact 176: 620–633 (1994).PubMedGoogle Scholar
  66. 66.
    Truchet G, Barker DG, Camut S, de Billy F, Vasse J, Huguet T: Alfalfa nodulation in the absence of Rhizobium. Mol Gen Genet 219: 65–68 (1989).CrossRefGoogle Scholar
  67. 67.
    Truchet G, Roche P, Lerouge P, Vasse J, Camut S, De Billy F, Promé J-C, Dénarié J: Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670–673 (1991).CrossRefGoogle Scholar
  68. 68.
    Van Brussel AAN, Recourt K, Pees E, Spaink HP, Tak T, Wijffelman CA, Kijne JW, Lugtenberg BJJ: A biovarspecific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. J Bact 172: 5394–5401 (1990).PubMedGoogle Scholar
  69. 69.
    Van Brussel AAN, Bakhuizen R, Van Spronsen P, Spaink HP, Tak T, Lugtenberg BJJ, Kijne J: Induction of preinfection thread structures in the host plant by lipooligosaccharides of Rhizobium. Science 257: 70–72 (1992).PubMedCrossRefGoogle Scholar
  70. 70.
    Velupillai P, Harn DA: Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsets. Proc Natl Acad Sci USA 91: 18–22 (1994).PubMedCrossRefGoogle Scholar
  71. 71.
    Vijn I, das Neves L, Van Kammen A, Franssen H, Bisseling T: Nod factors and nodulation in plants. Science 260: 1764–1765 (1993).PubMedCrossRefGoogle Scholar
  72. 72.
    Wagner GP, Lo J, Laine R, Almeder M: Chitin in the epidermal cuticle of a vertebrate (Paralipophrys trigloides, Blenniidae, Teleostei). Experientia 49: 317–319 (1993).CrossRefGoogle Scholar
  73. 73.
    Wagner GP: Evolution and multi-functionality of the chitin system. In: Molecular Approaches to Ecology and Evolution. Birkhäuser Verlag, Germany, in press.Google Scholar
  74. 74.
    Yang W-C, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, Van Kammen A, Bisseling T, Franssen H: Characterization of GmENOD40, agent showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3: 573–585 (1993).PubMedCrossRefGoogle Scholar
  75. 75.
    York WS, Darvill AG, Albersheim P: Inhibition of 2,4 dichlorophenoxyacetic acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide. Plant Physiol 75: 295–297 (1984).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1994

Authors and Affiliations

  • Herman P. Spaink
    • 1
  • Ben J. J. Lugtenberg
    • 1
  1. 1.Institute of Molecular Plant SciencesLeiden UniversityLeidenThe Netherlands

Personalised recommendations