Oligosaccharide Signalling Molecules

  • Robert A. Field


The signalling potential of plant carbohydrates had largely been overlooked until the last 2 decades. Whether trehalose- and sucrose-derived compounds, or oligosaccharides emanating from cell wall fragmentation, carbohydrate signals are thought to play key roles in plant growth and development at one level, and in activating plant defences against microbial infection at another. However, the literature is less than definitive, in many cases, about how in vitro observations correlate, or not, with true in vivo function. Nonetheless, a better understanding of the developmental regulation, allelopathic and defence-inducing properties of ‘oligosaccharin’ signalling carbohydrates offers scope not only for better understanding plant biology per se, but also presents novel opportunities for commercial exploitation. This chapter highlights oligosaccharide structures that have been reported to possess the properties of signal­ling molecules; although in many cases physiological relevance has not been demonstrated there is potential for exploitation.

This chapter outlines the main classes of plant-derived oligosaccharide molecules that have been reported to possess signalling capabilities. Comment is made on reports of the physiological function and/or the action of such compounds when fed exogenously. In many cases, whilst biological activity has been demonstrated its relevance to physiological function remains to be established.


Anthocyanin Biosynthetic Pathway Activate Plant Defence Carbon Metabolite Nuclear Proteome Tomato Pericarp 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Halford, N.G. and Paul, M.J. (2003). Carbon metabolite sensing and signalling. Plant Biotechnol. J. 1, 381–398.PubMedCrossRefGoogle Scholar
  2. 2.
    Gibson, S.I. (2004). Sugar and phytohormone response pathways: navigating a signalling network. J. Exp. Bot. 55, 253–264.PubMedCrossRefGoogle Scholar
  3. 3.
    Rook, F. and Bevan, M.W. (2003). Genetic approaches to understanding sugar-response pathways. J. Exp. Bot. 54, 495–501.PubMedCrossRefGoogle Scholar
  4. 4.
    Rook, F., Corke, F., Baier, M., Holman, R., May, A.G., and Bevan, M.W. (2006). Impaired sucrose induction1 encodes a conserved plant-specific protein that couples carbohydrate availability to gene expression and plant growth. Plant J. 46, 1045–1058.PubMedCrossRefGoogle Scholar
  5. 5.
    Gupta, A.K. and Kaur, N. (2005). Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J. Biosci. 30, 761–776.PubMedCrossRefGoogle Scholar
  6. 6.
    Lunn, J.E., Feil, R., Hendriks, J.H.M., Gibon, Y., Morcuende, R., Osuna, D., Scheible, W.R., Carillo, P., Hajirezaei, M.R., and Stitt, M. (2006). Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem. J. 397, 139–148.PubMedCrossRefGoogle Scholar
  7. 7.
    Bae, H., Herman, E., and Sicher, R. (2005). Endogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture. Plant Sci. 168, 1293–1301.CrossRefGoogle Scholar
  8. 8.
    Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., and Perata, P. (2006). Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 140, 637–646.PubMedCrossRefGoogle Scholar
  9. 9.
    Villalobo, A., Nogales-Gonzalez, A., and Gabius, H.J. (2006). A guide to signaling pathways connecting protein-glycan interaction with the emerging versatile effector functionality of mammalian lectins. Trends Glycosci. Glycotechnol. 18, 1–37.CrossRefGoogle Scholar
  10. 10.
    van Damme, E.J.M., Barre, A., Rouge, P., and Peumans, W.J. (2004). Cytoplasmic/nuclear plant lectins: a new story. Trends Plant Sci. 9, 484–489.PubMedCrossRefGoogle Scholar
  11. 11.
    Barre, A., Herve, C., Lescure, B., and Rouge, P. (2002). Lectin receptor kinases in plants. Crit. Rev. Biochem. 21, 379–399.Google Scholar
  12. 12.
    Dwek, R. A. (1996). Glycobiology: toward understanding the function of sugars. Chem. Rev. 96, 683–720.PubMedCrossRefGoogle Scholar
  13. 13.
    Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G., and Marth, J., Editors. (2009). Essentials of Glycobiology, 2nd edition, Cold Spring Harbor Laboratory Press, New York.Google Scholar
  14. 14.
    Gabius, H.J., Siebert, H. C., Andre, S., Jimenez-Barbero, J., and Rudiger, H. (2004). Chemical biology of the sugar code. ChemBioChem 5, 741–764.CrossRefGoogle Scholar
  15. 15.
    Sharon, N. and Lis, H. (2004). History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14, 53R–62R.PubMedCrossRefGoogle Scholar
  16. 16.
    Ambrosi, M., Cameron, N.R., and Davis, B.G. (2005). Lectins: tools for the molecular understanding of the glycocode. Org. Biomol. Chem. 3, 1593–1608.PubMedCrossRefGoogle Scholar
  17. 17.
    Albersheim, P. and Darvill, A.G. (1985). Oligosaccharins: novel molecules that can regulate growth, development, reproduction, and defense against disease in plants. Sci. Am. 253, 58–64.CrossRefGoogle Scholar
  18. 18.
    Albersheim, P., Augur, C., Cheong, J.-J., Eberhard, S., Hahn, M.G., Marfa, V., Mohnen, D., O’Neill, M.A., Spiro, M.D., York, W.S., and Darvill, A.G. (1992). Oligosaccharins -oligosaccharide regulatory molecules. Acc. Chem. Res. 25, 77–83.CrossRefGoogle Scholar
  19. 19.
    Ozeretskovskaya, O.L. and Romenskaya, I.G. (1996). Oligosaccharins as regulatory molecules of plants. Russ. J. Plant Physiol. 43, 648–655.Google Scholar
  20. 20.
    D’Haeze, W. and Holsters, M. (2002). Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12, 79R–105R.PubMedCrossRefGoogle Scholar
  21. 21.
    Rose, J.K., Ham, K.S., Darvill, A.G., and Albersheim P. (2002). Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14, 1329–1345.PubMedCrossRefGoogle Scholar
  22. 22.
    Laus, M.C. and Kijne, W.C. (2004). A fixer’s dress code: Surface polysaccharides and host-plant-specificity in the root nodule symbiosis. Trends Glycosci. Glycotechnol. 16, 281–290.CrossRefGoogle Scholar
  23. 23.
    Spaink, H.P. (2004). Specific recognition of bacteria by plant LysM domain receptor kinases. Trends Microbiol. 12, 201–204.PubMedCrossRefGoogle Scholar
  24. 24.
    Becker, A., Fraysse, N., and Sharypova, L. (2005). Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant-Microbe Interact 18, 899–905.PubMedCrossRefGoogle Scholar
  25. 25.
    Geurts, R., Fedorova, E., and Bisseling, T. (2005). Nod factor signalling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8, 346–352.PubMedCrossRefGoogle Scholar
  26. 26.
    Mulder, L., Lefebvre, B., Cullimore, J., and Imberty, A. (2006). LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors. Glycobiology 16, 801–809.PubMedCrossRefGoogle Scholar
  27. 27.
    Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., and Shibuya, N. (2006). Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci USA 103, 11086–11091.PubMedCrossRefGoogle Scholar
  28. 28.
    Damasceno, C.M.B., Bishop, J.G., Ripoll, D.R., Win, J., Kamoun, S., Rose, J.K.C. (2008). Structure of the glucanase inhibitor protein (GIP) family from Phytophthora species suggests coevolution with plant endo-β-1,3-glucanases. Mol. Plant-Microbe Interact. 21, 820–830.PubMedCrossRefGoogle Scholar
  29. 29.
    Aldington, S., McDougall, G.J., and Fry, S.C. (1991). Structure-activity relationships of biologically active oligosaccharides. Plant Cell Environ. 14, 625–636.CrossRefGoogle Scholar
  30. 30.
    Cote, F. and Hahn, M.G. (1994). Oligosacharins: structures and signal transduction. Plant Mol. Biol. 26, 1379–1411.PubMedCrossRefGoogle Scholar
  31. 31.
    Fry, S.C. (1996). Oligosaccharin mutants. Trends Plant Sci. 1, 326–328.Google Scholar
  32. 32.
    John, M., Rohrig, H., Schmidt, J., Walden, R., and Schell, J. (1997). Cell signalling by oligosaccharides. Trends Plant Sci. 2, 111–115.CrossRefGoogle Scholar
  33. 33.
    Cote, F., Ham, K.-S., Hahn, M.G., and Bergman, C.W. (1998). Oligosaccharide elicitors in host-pathogen interactions: generation, perception and signal transduction. In: Biswas, B.B. and Das, H. (Eds), Subcellular Biochemistry, Vol. 29, Plant-microbe interactions. Plenum Press, New York, pp. 385–431.Google Scholar
  34. 34.
    Dumville, J.C. and Fry, S.C. (2000). Uronic acid-containing oligosaccharins: their biosynthesis, degradation and signalling roles in non-diseased plant tissues. Plant Physiol. Biochem. 38, 125–140.CrossRefGoogle Scholar
  35. 35.
    Ridley, B.L., O’Neill, M.A., and Mohnen, D.A. (2001). Pectins: structure, biosynthesis, and oligogalacturonide-related signalling. Phytochemistry 57, 929–967.PubMedCrossRefGoogle Scholar
  36. 36.
    Brett, C. and Waldron, K. (1996). Physiology and Biochemistry of Plant Cell Walls, 2nd Edition, Chapman & Hall, London.Google Scholar
  37. 37.
    Carpita, N. and McCann, M. (2000). in: Buchanan, B.B., Gruissem, W., and Jones, R.L. (Eds) Biochemistry and Molecular Biology of Plants, American Society of Plant Biologists, Rockville, MD, pp. 52–109.Google Scholar
  38. 38.
    Somerville, C., Bauer, S., Brininstool, G., Facette, M., Hamann, T., Milne, J., Osborne, E., Paredez, A., Persson, S., Raab, T., Vorwerk, S., and Youngs, H. (2004). Toward a systems approach to understanding plant-cell walls. Science 306, 2206–2211.PubMedCrossRefGoogle Scholar
  39. 39.
    Fry, S.C. (2004). Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytologist 161, 641–675.CrossRefGoogle Scholar
  40. 40.
    Bishop, P.D., Makus, D.J., Pearce, G., and Ryan, C.A. (1981). Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymatically released from cell walls. Proc. Natl. Acad. Sci. USA 78, 3536–3540.PubMedCrossRefGoogle Scholar
  41. 41.
    Hahn, M.G., Darvill, A.G., and Albersheim, P. (1981). Host-pathogen interactions XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol. 68, 1161–1169.PubMedCrossRefGoogle Scholar
  42. 42.
    Decreux, A. and Messiaen, J. (2005). Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 46, 268–278.PubMedCrossRefGoogle Scholar
  43. 43.
    Decreux, A., Thomas, A., Spies, B., Brasseur, R., van Cutsem, P., and Messiaen, J. (2006). In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry 67, 1068–1079.PubMedCrossRefGoogle Scholar
  44. 44.
    Loreti, E., Bellincampi, D., Millet, C., Alpi, A., and Perata, P. (2002). Elicitors of defence responses repress a gibberellin signalling pathway in barley embryos. J. Plant Physiol. 159, 1383–1386.CrossRefGoogle Scholar
  45. 45.
    Casasoli, M., Meliciani, I., Cervone, F., De Lorenzo, G., and Mattei, B. (2007). Oligogalacturonide-induced changes in the nuclear proteome of Arabidopsis thaliana. Int. J. Mass Spectrom. 268, 277–282.CrossRefGoogle Scholar
  46. 46.
    Aziz, A., Heyraud, A., and Lambert, B. (2004). Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218, 767–774.PubMedCrossRefGoogle Scholar
  47. 47.
    Hasegawa, K., Mitzutani, J., Kosemura, S., and Yamamura, S. (1992). Isolation and identification of lepidimoide, a new allelopathic substance from mucilage of germinated cress seeds. Plant Physiol. 100, 1059–1061.PubMedCrossRefGoogle Scholar
  48. 48.
    Yamada, K., Anai, T., and Hasegawa, K. (1995). Lepidimoide, an allelopathic substance in the exudates from germinated seeds. Phytochemistry 39, 1031–1032.CrossRefGoogle Scholar
  49. 49.
    Yamada, K., Kosemura, S., Yamamura, S., and Hasegawa, K. (1997). Exudation of an allelopathic substance lepidimoide from seeds during germi­nation. Plant Growth Regul. 22, 189–192.CrossRefGoogle Scholar
  50. 50.
    Yokotani-Tomita, K., Goto, N., Kosemura, S., Yamamura, S., and Hasegawa, K. (1998). Growth-promoting allelopathic substance exuded from germinating Arabidopsis thaliana seeds. Phytochemistry 47, 1–2.PubMedCrossRefGoogle Scholar
  51. 51.
    Yamada, K., Anai, T., Kosemura, S., Yamamura, S., and Hasegawa, K. (1996). Structure activity relationship of lepidimoide and its analogues. Phytochemistry 41, 671–673.PubMedCrossRefGoogle Scholar
  52. 52.
    Tanaka, M., Yoshimura, M., Suto, M., Yokota, A., Asano, K., Sukara, E., and Tomita, F. (2002). Production of lepidimoide by an endophytic fungus from polysaccharide extracted from Abelmoschus sp.: identification of the product and the organism producing it. J. Biosci. Bioeng. 93, 531–536.PubMedGoogle Scholar
  53. 53.
    Saranpuetti, C., Tanaka, M., Sone, T., Asano, K., and Tomita, F. (2006). Determination of enzymes from Colletotrichum sp AHU9748 essential for lepidimoide production from okra polysaccharide. J. Biosci. Bioeng. 102, 452–456.PubMedCrossRefGoogle Scholar
  54. 54.
    Ochiai, A., Itoh, T., Kawamata, A., Hashimoto, W., and Murata, K. (2007). Plant cell wall degradation by saprophytic Bacillus subtilis strains: Gene clusters responsible for rhamnogalacturonan depolymerization. Appl. Environ. Microbiol. 73, 3803–3813.PubMedCrossRefGoogle Scholar
  55. 55.
    McDougall, G.J. and Fry, S.C. (1991). Xyloglucan nonasaccharide, a naturally occurring oligosaccharin, arises in vivo by polysaccharide breakdown. J. Plant. Physiol. 137, 332–336.CrossRefGoogle Scholar
  56. 56.
    Fry, S.C., York, W.S., Albersheim, P., Darvill, A., Hayashi, T., Joseleau, J.P., Kato, Y., Lorences, E.P., Maclachlan, G.A., McNeil, M., Mort, A.J., Reid, J.S.G., Seitz, H.U., Selvendran, R.R., Voragen, A.G.J., and White, A.R. (1993). An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol. Plant. 89, 1–3.CrossRefGoogle Scholar
  57. 57.
    Warneck, H.M., Fulton, D.C., Seitz, H.U., and Fry, S.C. (1998). Transport, degradation and cell wall-integration of XXFGol, a growth-regulating nonasaccharide of xyloglucan, in pea stems. Planta 204, 78–85.CrossRefGoogle Scholar
  58. 58.
    Pavlova, Z.N., Ash, O.A., Vnuchkova, V.A., Babakov, A.V., Torgov, V.I., Nechaev, O.A., Usov, A.I., and Shibaev, V.N. (1992). Biological activity of a synthetic pentasaccharide fragment of xyloglucan. Plant Sci. 85, 131–134.CrossRefGoogle Scholar
  59. 59.
    Augur, C., Benhamou, N., Darvill, A., and Albersheim, P. (1993). Purification, characterization and cell wall localization of an α-fucosidase that inactivates a xyloglucan oligosaccharin. Plant J. 3, 415–426.PubMedCrossRefGoogle Scholar
  60. 60.
    Zabotin, A.I., Barisheva, T.S., Larskaya, I.A., Toroshina, T.E., Trofimova, O.V., Hahn, M.G., and Zabotina, O.A. (2005). Oligosaccharin – a new systemic factor in the acquisition of freeze tolerance in winter plants. Plant Biosyst. 139, 36–41.CrossRefGoogle Scholar
  61. 61.
    Zabotina, O.A., Ayupova, D.A., Toroshchina, T.E., and Zabotin, A.I. (2003). Involvement of oligosaccharides in adaptation of winter wheat seedlings to sub-zero temperatures. Biol. Bull. 30, 464–467.CrossRefGoogle Scholar
  62. 62.
    Auxtova, O., Liskova, D., Kakoniova, D., Kubackova, M., Karacsonyi, S., and Bilisics, L. (1995). Effect of galactoglucomannan-derived oligosaccharides on elongation growth of pea and spruce stem segments stimulated by auxin. Planta 196, 420–424.CrossRefGoogle Scholar
  63. 63.
    Kollarova, K., Liskova, D., and Capek, P. (2006). Further biological characteristics of galactoglucomannan oligosaccharides. Biol. Plant. 50, 232–238.CrossRefGoogle Scholar
  64. 64.
    Kollarova, K., Liskova, D., and Lux, A. (2007). Influence of galactoglucomannan oligosaccharides on root culture of Karwinskia humboldtiana. Plant Cell Tissue Organ Cult. 91, 9–19.CrossRefGoogle Scholar
  65. 65.
    VarelaNieto, I., Leon, Y., and Caro, H.N. (1996). Cell signalling by inositol phosphoglycans from different species. Comp. Biochem. Physiol. B. 115, 223–241.CrossRefGoogle Scholar
  66. 66.
    Ferguson, M.A.J. and Williams, A.F. (1988). Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu. Rev. Biochem. 57, 285–320.PubMedCrossRefGoogle Scholar
  67. 67.
    Smith, C.K., Hewage, C.M., Fry, S.C., and Sadler, I.H. (1999). α-D-Mannopyranosyl-(1,4)-α-D-glucuronopyranosyl-(1,2)-myo-inositol, a new and unusual oligosaccharide from cultured rose cells. Phytochemistry 52, 387–396.CrossRefGoogle Scholar
  68. 68.
    Smith, C.K. and Fry, S.C. (1999). Biosynthetic origin and longevity in vivo of α-D-mannopyranosyl-(1,4)-α-D-glucuronopyranosyl-(1,2)-myo-inositol, an unusual extracellular oligosaccharide produced by cultured rose cells. Planta 210, 150–156.PubMedCrossRefGoogle Scholar
  69. 69.
    Dumville, J.C. and Fry, S.C. (2003a, b). Gentiobiose: a novel oligosaccharin in ripening tomato fruit. Planta 216, 484–495; Planta 217, 346–348.PubMedGoogle Scholar
  70. 70.
    Helenius, A. and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364–2369.PubMedCrossRefGoogle Scholar
  71. 71.
    Durrant, C. and Moore, S.E.H. (2002). Perturbation of free oligosaccharide trafficking in endoplasmic reticulum glucosidase I-deficient and castanospermine-treated cells. Biochem. J. 365, 239–247.PubMedCrossRefGoogle Scholar
  72. 72.
    Alonzi, D.S., Neville, D.C.A., Lachmann, R.H., Dwek, R.A., and Butters, T.D. (2008). Glucosylated free oligosaccharides are biomarkers of endoplasmic reticulum α-glucosidase inhibition. Biochem. J. 409, 571–580.PubMedCrossRefGoogle Scholar
  73. 73.
    Wilson, I.B.H. (2002). Glycosylation of proteins in plants and invertebrates. Curr. Opin. Struct. Biol. 12, 569–577.PubMedCrossRefGoogle Scholar
  74. 74.
    Megumi, M. and Yoshinobu, K. (2005). N-Glycan metabolism and plant cell differentiation and growth. Trends Glycosci. Glycotechnol. 17, 205–214.CrossRefGoogle Scholar
  75. 75.
    Yunovitz, H. and Gross, K. C. (1994). Effect of tunicamycin on metabolism of unconjugated N-glycans in relation to regulation of tomato fruit ripening. Phytochemistry 37, 663–668.PubMedCrossRefGoogle Scholar
  76. 76.
    Yunovitz, H., Livsey, J.N., and Gross, K.C. (1996). Unconjugated Man5GlcNAc occurs in vegetative tissues of tomato. Phytochemistry 42, 607–610.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Biological ChemistryJohn Innes CentreNorwichUK

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