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Transport of Salicylic Acid and Related Compounds

  • J.-L. BonnemainEmail author
  • J.-F. Chollet
  • F. Rocher
Chapter

Abstract

Various stresses promote SA accumulation. SA is in part conjugated in the cytoplasm to inactive compounds such as salicylic acid O-β-glucoside (SAG) or modified to active compounds such as methylsalicylate (MeSA). SAG is sequestered in the vacuole by an ATP-binding cassette transporter mechanism or an H+-antiporter mechanism. Free SA is mobile and can be transported within the plant, mainly via the phloem. SA molecules found in the phloem sap may come from the synthesis area via the symplastic route in symplastic loaders or may be taken up from the phloem apoplast (apoplastic loaders). In this latter case, SA must cross the plasma membrane of the companion cell-sieve cell complex. Similarly, synthetic derivatives or analogs applied to the foliage to enhance plant defence must cross at least once the plasma membrane before reaching the sieve tubes. The ability of molecules to diffuse through the plasma membrane is dependent on their chemical properties (size of the molecule, Log D, polar surface area, number of hydrogen bond donors). On these bases, the discrepancies between the computed predictions of phloem mobility of SA and various analogs and the actual results, as well as the effect of pCMBS on uptake suggest that SA transport involves a pH-dependent carrier system in addition to the ion trap mechanism, at least in the cotyledons of Ricinus communis. Although SA levels increase in both the phloem and systemic leaves after mature leaf infection, this salicylate is clearly not the primary systemic signal which contributes to SAR. Several data strongly suggest that MeSA as well as azelaic acid and small lipids are earlier signals. As MeSA is predicted to be very poorly phloem mobile, the mechanism of long distance transport of this volatile compound remains to be elucidated.

Keywords

Salicylic acid Salicylic acid metabolites Salicylic acid analogs Cell compartmentation Long distance transport Ricinus model Diffusion predictors 

References

  1. Bental, Y., & Cleland, C. F. (1982). Uptake and metabolism of C-14 salicylic-acid in Lemna gibba G3. Plant Physiology, 70, 291–296.CrossRefGoogle Scholar
  2. Bhal, S. K., Kassam, K., Peirson, I. G., & Pearl, G. M. (2007). The rule of five revisited: Applying log D in place of log P in drug-likeness filters. Molecular Pharmaceutics, 4, 556–560.PubMedCrossRefGoogle Scholar
  3. Bostock, R. M. (2005). Signal crosstalk and induced resistance: Straddling the line between cost and benefit. Annual review of Phytopathology, 43, 545–580.PubMedCrossRefGoogle Scholar
  4. Bouchepillon, S., Fleuratlessard, P., Fromont, J. C., Serrano, R., & Bonnemain, J. L. (1994). Immunolocalization of the plasma-membrane H+ -ATPase in minor veins of Vicia faba in relation to phloem loading. Plant Physiology, 105, 691–697.Google Scholar
  5. Bourquin, S., Bonnemain, J. L., & Delrot, S. (1990). Inhibition of loading of C-14 assimilates by para-chloromercuribenzenesulfonic acid: localization of the apoplastic pathway in Vicia faba. Plant Physiology, 92, 97–102.PubMedCrossRefGoogle Scholar
  6. Bromilow, R.H., Chamberlain, K., & Evans, A.A. (1991). Molecular structure and properties of xenobiotics in relation to phloem translocation. In J.L. Bonnemain, S. Delrot, W.J. Lucas, J. Dainty (Eds.), Recent advances in phloem transport and assimilate compartmentation (pp. 332–340). Cognac, France: Fourth International Conference on Phloem Transport and Assimilate Compartmentation, August 19–24, 1990. xiv + 344p. Ouest Editions, Nantes, France.Google Scholar
  7. Bush, D. R. (1993). Inhibitors of the proton-sucrose symport. Archives of Biochemistry and Biophysics, 307, 355–360.PubMedCrossRefGoogle Scholar
  8. Champigny, M. J., & Cameron, R. K. (2009). Action at a distance: Long-distance signals in induced resistance. In L. C. VanLoon (Ed.), Advances in botanical research (Vol. 51, pp. 123–171). London: Elsevier.Google Scholar
  9. Chen, H. J., Hou, W. C., Kuc, J., & Lin, Y. H. (2001). Ca2+ -dependent and Ca2+ -independent excretion modes of salicylic acid in tobacco cell suspension culture. Journal of Experimental Botany, 52, 1219–1226.PubMedCrossRefGoogle Scholar
  10. Clarke, A., Mur, L. A., Darby, R. M., & Kenton, P. (2005). Harpin modulates the accumulation of salicylic acid by Arabidopsis cells via apoplastic alkalization. Journal of Experimental Botany, 56, 3129–3136.PubMedCrossRefGoogle Scholar
  11. Dean, J. V., & Mills, J. D. (2004). Uptake of salicylic acid 2-O-beta-d-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiologia Plantarum, 120, 603–612.PubMedCrossRefGoogle Scholar
  12. Dean, J. V., Mohammed, L. A., & Fitzpatrick, T. (2005). The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta, 221, 287–296.PubMedCrossRefGoogle Scholar
  13. Delrot, S., & Bonnemain, J. L. (1981). Involvement of protons as a substrate for the sucrose carrier during phloem loading in Vicia faba leaves. Plant Physiology, 67, 560–564.PubMedCrossRefGoogle Scholar
  14. Delrot, S., Despeghel, J., & Bonnemain, J. (1980). Phloem loading in Vicia faba leaves: Effect of N-ethylmaleimide and parachloromercuribenzenesulfonic acid on H+ extrusion, K+ and sucrose uptake. Planta, 149, 144–148.CrossRefGoogle Scholar
  15. DeWitt, N. D., & Sussman, M. R. (1995). Immunocytological localization of an epitope-tagged plasma membrane proton pump (H+ -ATPase) in phloem companion cells. Plant Cell, 7, 2053–2067.PubMedGoogle Scholar
  16. Dinant, S., Bonnemain, J. L., Girousse, C., & Kehr, J. (2010). Phloem sap intricacy and interplay with aphid feeding. Comptes Rendus Biologies, 333, 504–515.PubMedCrossRefGoogle Scholar
  17. Enerson, B. E., & Drewes, L. R. (2003). Molecular features, regulation, and function of monocarboxylate transporters: implications for drug delivery. Journal of Pharmaceutical Sciences, 92, 1531–1544.PubMedCrossRefGoogle Scholar
  18. Enyedi, A. J., Yalpani, N., Silverman, P., & Raskin, I. (1992). Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proceedings of the National Academy of Sciences, 89, 2480–2484.CrossRefGoogle Scholar
  19. Ertl, P., Rohde, B., & Selzer, P. (2000). Fast calculation of molecular polar surface area as a sum of fragment-based contributions and its application to the prediction of drug transport properties. Journal of Medicinal Chemistry, 43, 3714–3717.PubMedCrossRefGoogle Scholar
  20. Ferguson, A. R., Eiseman, J. A., & Leonard, J. A. (1983). Xylem sap from Actinidia Chinensis: seasonal changes in composition. Annals of Botany, 51, 823–833.Google Scholar
  21. Fromard, L., Babin, V., Fleuratlessard, P., Fromont, J. C., Serrano, R., & Bonnemain, J. L. (1995). Control of vascular sap ph by the vessel associated cells in woody species: physiological and immunological studies. Plant Physiology, 108, 913–918.PubMedGoogle Scholar
  22. Gamalei, Y. (1989). Structure and function of leaf minor veins in trees and herbs. A taxonomic review. Trees Structure and Function, 3, 96–110.CrossRefGoogle Scholar
  23. Giaquinta, R. (1977). Possible role of pH gradient and membrane ATPase in loading of sucrose into sieve tubes. Nature, 267, 369–370.CrossRefGoogle Scholar
  24. Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., et al. (2010). Compatible plant-aphid interactions: How aphids manipulate plant responses. Comptes Rendus Biologies, 333, 516–523.PubMedCrossRefGoogle Scholar
  25. Harborne, J. (1980). Plant phenolics. In: A. Bell, B. Charlwood (Eds.), Encyclopedia of Plant Physiology. New Series (pp. 329–402). Vol 8. Secondary plant products. Berlin: Springer.Google Scholar
  26. Hsu, F. C., & Kleier, D. A. (1996). Phloem mobility of xenobiotics VIII. A short review. Journal of Experimental Botany, 47, 1265–1271.PubMedCrossRefGoogle Scholar
  27. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J., & Greenberg, J. T. (2009). Priming in systemic plant immunity. Science, 324, 89–91.PubMedCrossRefGoogle Scholar
  28. Kawano, T., Furuichi, T., & Muto, S. (2004). Controlled salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotechnology, 21, 319–335.CrossRefGoogle Scholar
  29. Kiefer, I. W., & Slusarenko, A. J. (2003). The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiology, 132, 840–847.PubMedCrossRefGoogle Scholar
  30. Kleier, D. A. (1988). Phloem mobility of xenobiotics 1. mathematical model unifying the weak acid and intermediate permeability theories. Plant Physiology, 86, 803–810.PubMedCrossRefGoogle Scholar
  31. Kleier, D. A., & Hsu, F. C. (1996). Phloem mobility of xenobiotics. 7. The design of phloem systemic pesticides. Weed Science, 44, 749–756.Google Scholar
  32. Koljonen, M., Rousu, K., Cierny, J., Kaukonen, A. M., & Hirvonen, J. (2008). Transport evaluation of salicylic acid and structurally related compounds across Caco-2 cell monolayers and artificial PAMPA membranes. European Journal of Pharmaceutics and Biopharmaceutics, 70, 531–538.PubMedCrossRefGoogle Scholar
  33. Lemoine, R. (2000). Sucrose transporters in plants: update on function and structure. Biochimica et Biophysica Acta, 1465, 246–262.PubMedCrossRefGoogle Scholar
  34. Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (1997). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advance Drug Delivery Review, 23, 3–25.CrossRefGoogle Scholar
  35. Liu, P. P., von Dahl, C. C., Park, S. W., & Klessig, D. F. (2011). Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiology, 155, 1762–1768.PubMedCrossRefGoogle Scholar
  36. Malamy, J., Carr, J. P., Klessig, D. F., & Raskin, I. (1990). Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002–1004.PubMedCrossRefGoogle Scholar
  37. Metraux, J. P., Signer, H., Ryals, J., Ward, E., Wyssbenz, M., Gaudin, J., et al. (1990). Increase in salicylic-acid at the onset of systemic acquired-resistance in cucumber. Science, 250, 1004–1006.PubMedCrossRefGoogle Scholar
  38. Molders, W., Buchala, A., & Metraux, J. P. (1996). Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiology, 112, 787–792.PubMedGoogle Scholar
  39. Oparka, K. J. (1991). Uptake and compartmentation of fluorescent probes by plant cells. Journal of Experimental Botany, 42, 565–579.CrossRefGoogle Scholar
  40. Orlich, G., & Komor, E. (1992). Phloem loading in Ricinus cotyledons: sucrose pathways via the mesophyll and the apoplasm. Planta, 187, 460–474.CrossRefGoogle Scholar
  41. Palm, K., Luthman, K., Ungell, A. L., Strandlund, G., Beigi, F., Lundahl, P., et al. (1998). Evaluation of dynamic polar molecular surface area as predictor of drug absorption: comparison with other computational and experimental predictors. Journal of Medicinal Chemistry, 41, 5382–5392.PubMedCrossRefGoogle Scholar
  42. Palm, K., Stenberg, P., Luthman, K., & Artursson, P. (1997). Polar molecular surface properties predict the intestinal absorption of drugs in humans. Pharmaceutical Research, 14, 568–571.PubMedCrossRefGoogle Scholar
  43. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., & Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318, 113–116.PubMedCrossRefGoogle Scholar
  44. Qian, Z. G., Zhao, Z. J., Xu, Y. F., Qian, X. H., & Zhong, J. J. (2006). Novel chemically synthesized salicylate derivative as an effective elicitor for inducing the biosynthesis of plant secondary metabolites. Biotechnology Progress, 22, 331–333.PubMedCrossRefGoogle Scholar
  45. Raskin, I. (1992a). Role of salicylic acid in plants. Annual Review of Plant Physiology Plant Molecular Biology, 43, 439–463.CrossRefGoogle Scholar
  46. Raskin, I. (1992b). Salicylate, a new plant hormone. Plant Physiology, 99, 799–803.PubMedCrossRefGoogle Scholar
  47. Raskin, I., Ehmann, A., Melander, W. R., & Meeuse, B. J. D. (1987). Salicylic-acid: a natural inducer of heat production in arum lilies. Science, 237, 1601–1602.PubMedCrossRefGoogle Scholar
  48. Rasmussen, J. B., Hammerschmidt, R., & Zook, M. N. (1991). Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiology, 97, 1342–1347.PubMedCrossRefGoogle Scholar
  49. Ratzinger, A., Riediger, N., von Tiedemann, A., & Karlovsky, P. (2009). Salicylic acid and salicylic acid glucoside in xylem sap of Brassica napus infected with Verticillium longisporum. Journal of Plant Research, 122, 571–579.PubMedCrossRefGoogle Scholar
  50. Rocher, F., Chollet, J. F., Jousse, C., & Bonnemain, J. L. (2006). Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiology, 141, 1684–1693.PubMedCrossRefGoogle Scholar
  51. Rocher, F., Chollet, J. F., Legros, S., Jousse, C., Lemoine, R., Faucher, M., et al. (2009). Salicylic acid transport in Ricinus communis involves a pH-dependent carrier system in addition to diffusion. Plant Physiology, 150, 2081–2091.PubMedCrossRefGoogle Scholar
  52. Seo, S., Ishizuka, K., & Ohashi, Y. (1995). Induction of salicylic acid beta-glucosidase in tobacco leaves by exogenous salicylic acid. Plant and Cell Physiology, 36, 447–453.Google Scholar
  53. Shulaev, V., Leon, J., & Raskin, I. (1995). Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell, 7, 1691–1701.PubMedGoogle Scholar
  54. Tamai, I., Takanaga, H., Maeda, H., Sai, Y., Ogihara, T., Higashida, H., et al. (1995). Participation of a proton-cotransporter, MCT1, in the intestinal transport of monocarboxylic acids. Biochemical and Biophysical Research Communications, 214, 482–489.PubMedCrossRefGoogle Scholar
  55. Tanaka, K., Zhou, F. F., Kuze, K., & You, G. F. (2004). Cysteine residues in the organic anion transporter mOAT1. Biochemical Journal, 380, 283–287.PubMedCrossRefGoogle Scholar
  56. Thomas, D. S., & Eamus, D. (2002). Seasonal patterns of xylem sap pH, xylem abscisic acid concentration, leaf water potential and stomatal conductance of six evergreen and deciduous Australian savanna tree species. Australian Journal of Botany, 50, 229–236.CrossRefGoogle Scholar
  57. Truman, W., Bennettt, M. H., Kubigsteltig, I., Turnbull, C., & Grant, M. (2007). Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences, 104, 1075–1080.CrossRefGoogle Scholar
  58. Turgeon, R. (2010). The Role of Phloem Loading Reconsidered. Plant Physiology, 152, 1817–1823.PubMedCrossRefGoogle Scholar
  59. Van Bel, A. (1993). Strategies of phloem loading. Annual Review of Plant Biology, 44, 253–281.CrossRefGoogle Scholar
  60. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditzjawhar, R., Ward, E., et al. (1994). Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell, 6, 959–965.PubMedGoogle Scholar
  61. Wang, L. J., Huang, W. D., Zhan, J. C., & Yu, F. Y. (2004). The transport of 14C-salicylic acid in heat-stressed young Vitis vinifera plants. Russian Journal of Plant Physiology, 51, 194–197.CrossRefGoogle Scholar
  62. White, R. F. (1979). Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology, 99, 410–412.PubMedCrossRefGoogle Scholar
  63. Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562–565.PubMedCrossRefGoogle Scholar
  64. Wilkinson, S. (1999). PH as a stress signal. Plant Growth Regulation, 29, 87–99.CrossRefGoogle Scholar
  65. Winiwarter, S., Ax, F., Lennernas, H., Hallberg, A., Pettersson, C., & Karlen, A. (2003). Hydrogen bonding descriptors in the prediction of human in vivo intestinal permeability. Journal of Molecular Graphics and Modelling, 21, 273–287.PubMedCrossRefGoogle Scholar
  66. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D. A., & Raskin, I. (1991). Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus infected tobacco. Plant Cell, 3, 809–818.PubMedGoogle Scholar
  67. Zarate, S. I., Kempema, L. A., & Walling, L. L. (2007). Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology, 143, 866–875.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Laboratoire Écologie et Biologie des InteractionsUniversité de Poitiers, Unité Mixte de Recherche CNRS 7267Poitiers cedexFrance
  2. 2.Institut de Chimie des Milieux et des Matériaux de PoitiersUniversité de Poitiers, Unité Mixte de Recherche CNRS 7285Poitiers cedexFrance

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