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Impact of Salicylic Acid on the Transport and Distribution of Sugars in Plants

  • M. S. KrasavinaEmail author
  • N. A. Burmistrova
Chapter
  • 2.1k Downloads

Abstract

The article discusses the ways of salicylic acid influence on transport of sucrose and its distribution in plants. The intercellular and long-distance transport along phloem depends on the presence or absence of SA. As a result of sucrose influx in heterotrophic tissues the content of sucrose in the sink organs may increase. Complex interactions between SA, sucrose, Ca2+, ROS and transmembrane electrical potential that occur in the apoplast and at the level of plasma membrane are discussed.

Keywords

Salicylic acid  Sucrose Cell-to-cell transport  Phloem transport  Electric potential  

References

  1. Aaziz, R., Dinant, S., & Epel, B. L. (2001). Plasmodesmata and plant cytoskeleton. Trends in Plant Science, 6, 326–330.PubMedGoogle Scholar
  2. Abdel-Wahed, M. S. A., Amin, A. A., & El-Rashad, S. M. (2006). Physiological effect of some bioregulators on vegetative growth, yield and chemical constituents of yellow maize plants. World Journal of Agricultural Science, 2, 149–155.Google Scholar
  3. Aldesuquy, H. S., Abo-Hamed, S. A., Abbas, M. A., & Elhakem, A. H. (2012). Role of glycine betaine and salicylic acid in improving growth vigour and physiological aspects of droughted wheat cultivars. Journal of Stress Physiology and Biochemistry, 8, 149–171.Google Scholar
  4. Al-Hakimi, A. M. A., & Alghalibis, S. M. S. (2007). Thiamin and salicylic acid as biological alternatives for controlling broad bean rot disease. Journal of Applied Science and Environmental Management, 11, 125–131.Google Scholar
  5. Allen, G. J., Chu, S. P., Harrington, C. L., Schumacher, K., Hoffmann, T., Tang, Y. Y., et al. (2001). A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature, 411, 1053–1057.PubMedGoogle Scholar
  6. Alpaslan, M., & Gunes, A. (2001). Interactive effects of boron and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants. Plant and Soil, 236, 123–128.Google Scholar
  7. Amin, A. A., Rashad, E.-S. M., & Gharib, F. A. E. (2008). Changes in morphological, physiological and reproductive characters of wheat plants as affected by foliar application with salicylic acid and ascorbic acid. Australian Journal of Basic and Applied Sciences, 2, 252–261.Google Scholar
  8. Anderson, J. M. (1983). Release of sucrose from Vicia faba L. leaf discs. Plant Physiology, 71, 333–340.Google Scholar
  9. Amin, A. A., Rashad, E.-S. M., & El-Abagy, H. M. H. (2007). Physiological effect of indole-3-butyric acid and salicylic acid on growth, yield and chemical constituents of onion plants. Journal of Applied Science Research, 3, 1554–1563.Google Scholar
  10. Arfan, M., Athar, H. R., & Ashraf, M. (2007). Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? Journal of Plant Physiology, 164, 685–694.PubMedGoogle Scholar
  11. Arimura, G., & Maffei, M. E. (2010). Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochemical and Biophysical Research Communications, 400, 455–460.PubMedGoogle Scholar
  12. Ayre, B. G. (2011). Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Molecular plant, 4, 377–394.PubMedGoogle Scholar
  13. Baghizadeh, G. A., Haj, R. M., & Mozafarih, H. (2009). Evaluation of interaction effect of drought stress with ascorbate and salicylic acid on some of physiological and biochemical parameters in Okra (Hibiscus esculentus L.). Research Journal of Biological Sciences, 4, 380–387.Google Scholar
  14. Baluška, F., Šamaj, J., Napier, R., & Volkmann, D. (1999). Maize calreticulin localizes preferentially to plasmodesmata in root apex. The Plant Journal, 19, 481–488.PubMedGoogle Scholar
  15. Baluška, F., Cvrckova, F., Kendrick-Jones, J., & Volkmann, D. (2001). Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiology, 126, 39–46.PubMedGoogle Scholar
  16. Baluška, F., Hlavacka, A., Volkmann, D., & Menzel, D. (2004). Getting connected: Actinbased cell-to-cell channels in plants and animals. Trends in Cell Biology, 14, 404–408.PubMedGoogle Scholar
  17. Barakat, N. A. M. (2011). Oxidative stress markers and antioxidant potential of wheat treated with phytohormones under salinity stress. Journal of Stress Physiology and Biochemistry, 7, 250–267.Google Scholar
  18. Barratt, D. H., Kölling, K., Graf, A., Pike, M., Calder, G., Findlay, K., et al. (2011). Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiology, 155, 328–341.PubMedGoogle Scholar
  19. Bayat, H., Alirezaie, M., & Neamati, H. (2012). Impact of exogenous salicylic acid on growth and ornamental characteristics of calendula (Calendula officinalis L.) under salinity stress. Journal of Stress Physiology and Biochemistry, 8, 258–267.Google Scholar
  20. Bayer, E., Thomas, C., & Maule, A. (2008). Symplastic domains in the Arabidopsis shoot apical meristem correlate with PDLP1 expression patterns. Plant Signaling & Behavior, 3, 853–855 Google Scholar
  21. Benitez-Alfonso, Y., Faulkner, C., Ritzenthaler, C., & Maule, A. J. (2010). Plasmodesmata: Gateways to local and systemic virus infection. Molecular Plant-Microbe Interactions, 23, 1403–1412.PubMedGoogle Scholar
  22. Bernard, F., Baghai, M., & Kaveh, S. H. (2012). In vitro carbohydrate stress: Salicylic acid increases soluble invertase activity in Pestacia vera L. in vitro plantlets. Iranian Journal of Plant Physiology, 2, 355–360.Google Scholar
  23. Bhuja, P., McLachlan, K., Stephens, J., & Taylor, G. (2004). Accumulation of ß-1,3-glucans, in response to aluminum and cytosolic calcium in Triticum aestivum. Plant and Cell Physiology, 45, 543–549.PubMedGoogle Scholar
  24. Blackman, L. M., & Overall, R. L. (1998). Immunolocalization of the cytoskeleton to plasmodesmata of Chara coralline. The Plant Journal, 14, 733–741.Google Scholar
  25. Botha, C. E. J., & Cross, R. H. M. (2000). Toward reconciliation of structure with function in plasmodesmata: Who is the gatekeeper. Micron, 31, 713–721.PubMedGoogle Scholar
  26. Burch-Smith, T. M., Stonebloom, S., Xu, M., & Zambryski, P. C. (2011). Plasmodesmata during development: Re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma, 248, 61–74.PubMedGoogle Scholar
  27. Burch-Smith, T. M., & Zambryski, P. C. (2012). Plasmodesmata paradigm shift: Regulation from without versus within. Annual Review of Plant Biology, 63, 239–260.PubMedGoogle Scholar
  28. Burmistrova, N. A., Krasavina, M. S., & Akanov, E. N. (2009). Salicylic acid can regulate phloem unloading in the root tip. Russian Journal of Plant Physiology, 56, 627–634.Google Scholar
  29. Carpaneto, A., Geiger, D., Bamberg, E., Sauer, N., Fromm, J., & Hedrich, R. (2005). Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. Journal of Biological Chemistry, 280, 21437–21443.PubMedGoogle Scholar
  30. Chapleo, S., & Hall, J. L. (1989). Sugar unloading in roots of Ricinus communis L. II. Characteristics of the extravascular apoplast. New Phytologist, 111, 381–390.Google Scholar
  31. Chaudhuri, B., Hormann, F., Lalonde, S., Brady, S. M., Orlando, D. A., Benfey, P., et al. (2008). Protonophore- and pH insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. The Plant Journal, 56, 948–962.PubMedGoogle Scholar
  32. Chen, L. Q., Qu, X. Q., Hou, B. H., Sosso, D., Osorio, S., Fernie, A. R., et al. (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science, 335, 207–211.PubMedGoogle Scholar
  33. Couée, I., Sulmon, C., Gouesbet, G., & El Amrani, A. (2006). Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany, 57, 449–459.PubMedGoogle Scholar
  34. Cronshaw, J., & Esau, K. (1968). P-protein in the phloem of Cucurbita. II. The P-protein of mature sieve elements. Journal of Cell Biology, 38, 292–303.PubMedGoogle Scholar
  35. Currier, H., & Webster, D. H. (1964). Callose formation and subsequent disappearance: Studies in ultrasound stimulation. Plant Physiology, 39, 843–847.PubMedGoogle Scholar
  36. Ding, B., Kwon, M. O., & Warnberg, L. (1996). Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. The Plant Journal, 10, 157–164.Google Scholar
  37. Dong, M. A., Farréb, E. M., & Thomashow, M. F. (2011). CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis. PNAS, 108, 7241–7246.PubMedGoogle Scholar
  38. Dong, X., Hong, Z., Chatterjee, J., Kim, S., & Verma, D. P. (2008). Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta, 229, 87–98.PubMedGoogle Scholar
  39. Ehlers, K., & van Bel, A. J. (2010). Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta, 231, 371–385.PubMedGoogle Scholar
  40. El Tayeb, M. A., & Ahmed, N. L. (2010). Response of wheat cultivars to drought and salicylic acid. American-Eurasian Journal of Agronomy, 3, 1–7.Google Scholar
  41. Esau, K., & Thorsch, J. (1985). Sieve plate pores and plasmodesmata, the communication channels of the symplast: Ultrastructural aspects and developmental relations. American Journal of Botany, 72, 1641–1653.Google Scholar
  42. Eschrich, W. (1965). Physiologie der Siebröhren callose. Planta, 65, 280–300.Google Scholar
  43. Evert, R. F., & Derr, W. F. (1964). Callose substance in sieve elements. American Journal of Botany, 51, 552–559.Google Scholar
  44. Farouk, S., & Osman, M. A. (2011). The effect of plant defense elicitors on common bean (Phaseolus vulgaris L.) growth and yield in absence or presence of spider mite (Tetranychus urticae Koch) infestation. Journal of Stress Physiology and Biochemistry, 7, 5–22.Google Scholar
  45. Farouk, S., Ghoneem, K. M., & Abeer, A. (2008). Induction and expression of systematic resistance to downy mildew disease in cucumber plant by elicitors. Egyptian Journal of Phytopathology, 1–2, 95–111.Google Scholar
  46. Fernandez-Calvino, L., Faulkner, C., Walshaw, J., Saalbach, G., Bayer, E., Benitez-Alfonco, Y., et al. (2011). Arabidopsis plasmodesmal proteome. PLoS ONE, 6, 1–13.Google Scholar
  47. Foyer, C. H., & Noctor, G. (2003). Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum, 119, 355–364.Google Scholar
  48. Froelich, D. R., Mullendore, D. L., Jensen, K. H., Ross-Elliott, T. J., Anstead, J. A., Thompson, G. A., et al. (2011). Phloem ultrastructure and pressure flow: Sieve-element-occlusion-related agglomerations do not affect translocation. Plant Cell, 23, 428–445.Google Scholar
  49. Furch, A. C. U., Zimmermann, M. R., Will, T., Hafke, J. B., & van Bel, A. J. E. (2010). Remote controlled stop of mass flow by biphasic occlusion in Cucurbita maxima. Journal of Experimental Botany, 61, 3697–3708.PubMedGoogle Scholar
  50. Gadi, B. R., & Laxmi, V. (2012). Effect of salicylic acid and moisture stress on sugar content and sucrose synthase activity in Ziziphus seedlings. Biochemical and Cellular Archives, 12, 21–23.Google Scholar
  51. Gamalei, Yu.V. (2004). Transport system of vascular plants. Publ. House S.-Petersburg State Uni, 422p.Google Scholar
  52. Gharib, F. A., & Hegazi, A. Z. (2010). Salicylic acid ameliorates germination, seedling growth, phytohormone and enzyme activity in bean (Phaseolus vulgaris L.) under cold stress. Journal of the American Science, 6, 675–683.Google Scholar
  53. Ghasemzadeh, A., & Jaafar, H. Z. E. (2012). Effect of salicylic acid application on biochemical changes in ginger (Zingiber officinale Roscoe). Journal of Medicinal Plants Research, 6, 790–795.Google Scholar
  54. Glass, A. D. M., & Dunlop, J. (1974). Influence of phenolic acids on ion uptake. IV. Depolarization of the membrane potentials. Plant Physiology, 54, 855–858.Google Scholar
  55. Giaquinta, R. T. (1977). Phloem loading of sucrose: pH dependence and selectivity. Plant Physiology, 59, 750–753.PubMedGoogle Scholar
  56. Giaquinta, R. T. (1979). Phloem loading of sucrose: Involvement of membrane ATPase and proton transport. Plant Physiology, 63, 744–748.PubMedGoogle Scholar
  57. Gordon, L. Kh., Minibayeva, F. V., Ogorodnikova, T. I., Rakhmatullina, D. F., Tzentzevitzky, A. N., Kolesnikov, O. P., et al. (2002). Salicylic acid induces dissipation of the proton gradient on the plant cell plasma membrane. Doklady Biological Sciences, 387, 581–583.PubMedGoogle Scholar
  58. Guan, H. P., & Janes, H. W. (1989). Sugar uptake in the protoplasts isolated from tomato leaves. Journal of Plant Physiology, 134, 327–330.Google Scholar
  59. Gunes, A., Inal, A., Alpaslan, M., Cicek, N., Guneri, E., Eraslan, F., et al. (2005). Effects of exogenously applied salicylic acid on the induction of multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Archives of Agronomy and Soil Science, 51, 687–695.Google Scholar
  60. Gutierrez–Coronado, M. A., Trejo-Lopez, C., & Larque-Saavedra, A. (1998). Effects of salicylic acid on growth of roots and shoots in soybean. Plant Physiology and Biochemistry, 36, 653–665.Google Scholar
  61. Hafke, J. B., Furch, A. C., Fricker, M. D., & van Bel, A. J. (2009). Forisome dispersion in Vicia faba is triggered by Ca(2+) hotspots created by concerted action of diverse Ca2+ channels in sieve elements. Plant Signaling & Behavior, 4, 968–972.Google Scholar
  62. Haroun, S. A., Aldesuqy, H. S., Shukry, W. M., & Gaber, A. M. (1998). Regulation of growth and metabolism in Lupinus termis plant by sodium salicylate. Egyptian Journal of Physiology Sciences, 22, 75–95.Google Scholar
  63. Hayat, S., Ali B., & Ahmad, A. (2007). Salicylic acid: Biosynthesis, metabolism and physiological role in plants. In: S. Hayat, A. & Ahmad (Eds.), Salicylic acid: A plant hormone (pp. 1–14). Dordrecht: Springer.Google Scholar
  64. Hayat, Q., Hayat, S., Irfan, M., & Ahmad, A. (2010). Effect of exogenous salicylic acid under changing environment. A review. Environmental and Experimental Botany, 68, 14–25.Google Scholar
  65. Hayat, S., Fariduddin, Q., Ali, B., & Ahmad, A. (2005). Effect of salicylic acid on growth and enzyme activities of wheat seedlings. Acta Agronomica Hungarica, 53, 433–437.Google Scholar
  66. Heinlein, M., & Epel, B. L. (2004). Macromolecular transport and signaling through plasmodesmata. International Review of Cytology, 235, 93–164.PubMedGoogle Scholar
  67. Herbers, K., Meuwly, P., Métraux, J.-P., & Sonnewald, U. (1996). Salicylic acid-independent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Letters, 397, 239–244.PubMedGoogle Scholar
  68. Holdaway-Clarke, T. L., Walker, N. A., Hepler, P. K., & Overall, R. L. (2000). Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta, 210, 329–335.PubMedGoogle Scholar
  69. Hunt, J. V., Dean, R. T., & Wolff, S. P. (1988). Hydroxyl radical production and autoxidative glycosylation. Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus and ageing. Biochemical Journal, 256, 205–212.PubMedGoogle Scholar
  70. Hussain, K., Nawaz, K., Majeed, A., Ilyas, U., Lin, F., Ali, K., et al. (2011). Role of exogenous salicylic acid applications for salt tolerance in violet. Sarhad Journal of Agriculture, 27, 171–175.Google Scholar
  71. Iqbal, M., & Ashraf, M. (2005). Changes in growth, Role of glycine betaine and salicylic acid, photosynthetic capacity and ionic relations in spring wheat (Triticum aestivum L.). Plant Growth Regulation, 60, 41–52.Google Scholar
  72. Iqbal, M., & Ashraf, M. (2006). Wheat seed priming in relation to salt toleration: Growth, yield and levels of free salicylic acid and polyamines. Annales Botanici Fennici, 43, 250–259.Google Scholar
  73. Jacobs, A. K., Lipka, V., Burton, R. A., Panstruga, R., Strizhov, N., Schulze-Lefert, P., et al. (2003). An Arabidopsis callose synthase, GSL 5, is required for wound and papillary callose formation. Plant Cell, 15, 2503–2513.PubMedGoogle Scholar
  74. Jayalakshmi, P., Suvarnalatha, D. P., Prasanna, N. D., Revathi, G., & Shaheen, S. K. (2010). Morphological and physiological changes of groundnut plants by foliar application with salicylic acid. Biosean, 5, 193–195.Google Scholar
  75. Kang, M. K., Park, K. S., & Choi, D. (1998). Coordinated expression of defense-related genes by TMV infection or salicylic acid treatment in tobacco. Molecules and Cells, 31, 388–392.Google Scholar
  76. Kartusch, R. (2003). On the mechanism of callose synthesis induction by metal ions in onion epidermal cells. Protoplasma, 220, 219–225.PubMedGoogle Scholar
  77. Kauss, H. (1985). Callose biosynthesis as a Ca2+-regulated process and possible relations to the induction of other metabolic changes. Journal of Cell Science. Supplement, 2, 89–103.PubMedGoogle Scholar
  78. Kaveh, S. H., Bernard, F., & Samiee, K. (2004). Growth stimulation and enhanced invertase activity induced by salicylic acid in tea cuttings (Camellia sinensis L.). In Proceedings of IV International Iran-Russia Conference (pp. 113–116).Google Scholar
  79. Kawano, T. (2003). Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports, 21, 829–837.PubMedGoogle Scholar
  80. Kawano, T., & Furuichi, T. (2007). Salicylic acid as a defense-related plant hormone. Roles of oxidative and calcium signaling paths in salicylic acid biology. In: S. Hayat & A. Ahmad (Eds.) Salicylic acid: A plant hormone (pp. 277–321). Dordrecht: Springer.Google Scholar
  81. Kawano, T., Nobuya, S., Takahashi, S., Uozumi, N., & Muto, S. (1998). Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: The earliest events in salicylic acid signal transduction. Plant and Cell Physiology, 39, 721–730.Google Scholar
  82. Keller, C. P., Barkosky, R. R., Seil, J. E., Mazurek, S. A., & Grundstad, M. L. (2008). The electrical response of Phaseolus vulgaris roots to abrupt exposure to hydroquinone. Plant Signaling & Behavior, 3, 633–640.Google Scholar
  83. Kempers, R., Ammerlaan, A., & van Bel, A. J. E. (1998). Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically loading species. Plant Physiology, 116, 271–278.Google Scholar
  84. Khan, S. U., Bano, A., & Jalal-ud-Din, G. A. (2012). Abscisic acid and salicylic acid seed treatment as potent inducer of drought tolerance in wheat (Triticum aestivum L.). Pakistan Journal of Botany, 44, 43–49, Special issue.Google Scholar
  85. Khan, W., Prithviraj, B., & Smith, D. L. (2003). Photosynthetic responses of corn and soybean to foliar application of salicylates. Journal of Plant Physiology, 160, 485–492.PubMedGoogle Scholar
  86. Khodary, S. E. A. (2004). Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants. International Journal of Agriculture & Biology, 6, 5–8.Google Scholar
  87. Klessig, D. F., & Malamy, J. (1994). The salicylic acid signal in plants. Plant Molecular Biology, 26, 1439–1458.PubMedGoogle Scholar
  88. Knoblauch, M., & van Bel, A. J. E. (1998). Sieve tubes in action. Plant Cell, 10, 35–50.Google Scholar
  89. Knoblauch, M., Stubenrauch, M., van Bel, A. J. E., & Peters, W. S. (2012). Forisome performance in artificial sieve tubes. Plant, Cell and Environment, 35, 1419–1427.PubMedGoogle Scholar
  90. Kobayashi, I., & Hakuno, H. (2003). Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta, 217, 340–345.PubMedGoogle Scholar
  91. Köhle, H., Jeblick, W., Poten, F., Blaschek, W., & Kauss, H. (1985). Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process. Plant Physiology, 77, 544–551.PubMedGoogle Scholar
  92. Krasavina, M. S. (2007). Effect of salicylic acid on solute transport in plants. In: S. Hayat & A. Ahmad (eds.) Salicylic acid: A plant hormone (pp. 25–68). Dordrecht: Springer.Google Scholar
  93. Krasavina, M. S., Ktitorova, I. N., & Burmistrova, N. A. (2001). Electrical conductance of cell-to-cell junctions and cytoskeleton of plant cells. Russian Journal of Plant Physiology, 48, 741–748.Google Scholar
  94. Krasavina, M. S., Malyshenko, S. I., Raldugina, G. N., Burmistrova, N. A., & Nosov, A. V. (2002). Can salicylic acid affect the intercellular transport of the tobacco mosaic virus by changing plasmodesmal permeability? Russian Journal of Plant Physiology, 49, 61–67.Google Scholar
  95. Kuhn, C., & Grof, C. P. L. (2010). Sucrose transporters of higher plants. Current Opinion in Plant Biology, 13, 288–298.PubMedGoogle Scholar
  96. Kuhn, C., Hajirezaei, M. R., Fernie, A. R., Roessner-Tunali, U., Czechowski, T., Hirner, B., et al. (2003). The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiology, 131, 102–113.PubMedGoogle Scholar
  97. Ladyzhenskaya, E. P., & Korablyova, N. P. (2011). Effect of salicylic acid on the proton translocation activity of plasmalemma of potato tuber cells. Applied Biochemistry and Microbiology, 47, 479–483. (in Russian).Google Scholar
  98. Lalonde, S., Wipf, D., & Frommer, W.B. (2004). Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology, 55, 341–372.Google Scholar
  99. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W. B., & Patrick, J. W. (2003). Phloem loading and unloading of sugars and amino acids. Plant, Cell and Environment, 26, 37–56.Google Scholar
  100. Lee, J. Y., Wang, X., Cui, W., Sage, R., Modla, S., Czymmek, K., et al. (2011). A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell, 23, 3353–3373.PubMedGoogle Scholar
  101. Lee, J. Y., & Lu, H. (2011). Plasmodesmata: The battle ground against intruders. Trends in Plant Science, 16, 201–210.PubMedGoogle Scholar
  102. Levy, A., Erlanger, M., Rosenthal, M., & Epel, B. L. (2007). A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. The Plant Journal, 49, 669–682.PubMedGoogle Scholar
  103. Liesche, J., & Schulz, A. (2012). In vivo quantification of cell coupling in plants with different phloem-loading strategies. Plant Physiology, 159, 355–365.PubMedGoogle Scholar
  104. Liu, Y., Liu, H., Pan, Q., Yang, H., Zhanm, J., & Huang, W. (2009a). The plasma membrane H+-ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves. Planta, 229, 1087–1098.PubMedGoogle Scholar
  105. Liu, Y., Zhang, J., Liu, H., & Huang, W. (2008). Salicylic acid or heat acclimation pre-treatment enhances the plasmamembrane-associated ATPase activities in young grape plants under heat shock. Scientia Horticulturae, 119, 21–27.Google Scholar
  106. Loutfy, N., El-Tayeb, M. A., Hassanen, A. M., Moustafa, M. F., Sakuma, Y., & Inouhe, M. (2012). Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). Journal of Plant Research, 125, 173–184.PubMedGoogle Scholar
  107. Lucas, W. J., & Lee, J.-Y. (2004). Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology, 5, 712–726.PubMedGoogle Scholar
  108. Lucas, W. J., Ham, B. K., & Kim, J. Y. (2009). Plasmodesmata—bridging the gap between neighboring plant cells. Trends in Cell Biology, 19, 495–503.PubMedGoogle Scholar
  109. Lyalin, O. O., Ktitorova, I. N., Barmicheva, E. M., & Achmedov, N. I. (1986). Intercellular connections in submersed trichomes of Salvinia. Fiziologia Rastenij, 33, 432–446. (in Russian).Google Scholar
  110. Maria, E. B., José, D. A., Maria, C. B., & Francisco, P. A. (2000). Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiologia Plantarum, 110, 503–511.Google Scholar
  111. Maslenkova, L., Peeva, V., Stojnova, Zh., & Popova, L. (2009). Salicylic acid-induced changes in photosystem II reactions in barley plants. Biotechnology and Biotechnological Equipment, 23, 297–300.Google Scholar
  112. Mathur, N., & Vyas, A. (2007). Physiological effect of some bioregulators on vegetative growth, yield and chemical constituents of pearl millet (Pennisetum typhoides (Burm) Stapf. and Hubb). International Journal of Agricultural Research, 2, 238–245.Google Scholar
  113. McAinsh, M. R., & Pittman, J. K. (2009). Shaping the calcium signature. New Phytologist, 181, 275–294.PubMedGoogle Scholar
  114. McNairn, R. B., & Currier, H. B. (1968). Translocation blockage by sieve plate callose. Planta, 82, 369–380.Google Scholar
  115. Minchin, P. E. H., & Thorpe, M. R. (1987). Measurement of unloading and reloading of photo-assimilate within the stem of bean. Journal of Experimental Botany, 38, 211–220.Google Scholar
  116. Mishra, A., & Choudhuri, M. A. (1999). Effect of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biologia Plantarum, 42, 409–415.Google Scholar
  117. Misra, N., & Saxena, P. (2009). Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Science, 177, 181–189.Google Scholar
  118. Morgan, J. M. (1994). Osmoregulation and water-stress in higher-plants. Annual Review of Plant Physiology, Plant Molecular Biology, 35, 299–319.Google Scholar
  119. Mostajeran, A., & Rahimi-Eichi, V. (2009). Effects of drought on growth and yield of rice (Oryza sativa L.) cultivars and accumulation of proline and soluble sugars in sheath and blades of their different age leaves. American-Eurasian Journal of Environmental Sciences, 5, 264–272.Google Scholar
  120. Mullendore, D. L., Windt, C. W., van As, H., & Knoblauch, M. (2010). Sieve tube geometry in relation to phloem flow. Plant Cell, 22, 579–593.Google Scholar
  121. Murphy, A. M., & Carr, J. P. (2002). Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiology, 128, 552–563.PubMedGoogle Scholar
  122. Najafian, S., Khoshkhui, M., Tavallali, V., & Saharkhiz, M. J. (2009). Effect of salicylic acid and salinity in thyme (Thymus vulgaris L.): Investigation on changes in gas exchange, water relations, and membrane stabilization and biomass accumulation. Australian Journal of Basic and Applied Sciences, 3, 2620–2626.Google Scholar
  123. Neuenschwander, U., Vernooij, B., Friedrich, L., Uknes, S., Kessmann, H., & Ryals, J. (1995). Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? The Plant Journal, 8, 227–233.Google Scholar
  124. Nishimura, M. T., Stein, M., Hou, B., Vogel, J. P., Edwards, H., & Somerville, S. C. (2003). Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science, 301, 969–972.PubMedGoogle Scholar
  125. Oparka, K. J., Duckett, C. M., Prior, D. A. M., & Fisher, D. M. (1994). Real time imaging of phloem unloading in the root tip of Arabidopsis. The Plant Journal, 5, 756–766.Google Scholar
  126. Oparka, K. J., & Roberts, A. G. (2001). Plasmodesmata. A not so open-and-shut case. Plant Physiology, 125, 123–126.PubMedGoogle Scholar
  127. Ostergaard, L., Petersen, M., Mattsson, O., & Mundy, J. (2002). An Arabidopsis callose synthase. Plant Molecular Biology, 49, 559–566.PubMedGoogle Scholar
  128. Patrick, J. W. (1997). Phloem unloading: sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology, Plant Molecular Biology, 28, 165–190.Google Scholar
  129. Pei, Z. M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G. J., et al. (2000). Calcium channels activated by hydrogen peroxidase mediate abscisic acid signaling in guard cells. Nature, 406, 731–734.PubMedGoogle Scholar
  130. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H. B., Lacy, M., Austin, M. J., Parker, J. E., Sharma, S. B., Klessig, D. F., Martienssen, R., Mattsson, O., Jensen, A. B., & Mundy, J. (2000). Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103, 1111–1120.Google Scholar
  131. Prudnikov, G. A., Panichkin, L. A., & Krasavina, M. S. (2010). Effect of ion channel blockers and H+-ATPase inhibitors on generation of local electrical response in a cucumber leaf. Russian Journal of Plant Physiology, 57, 865–874.Google Scholar
  132. Qudeimat, E., & Frank, W. (2009). Ca2+ signatures: the role of Ca2+-ATPases. Plant Signaling & Behavior, 4, 350–352.Google Scholar
  133. Radford, J. E., Vesk, M., & Overall, R. L. (1998). Callose deposition at plasmodesmata. Protoplasma, 201, 30–37.Google Scholar
  134. Rai, V. K., Sharma, S. S., & Sharma, S. (1986). Reversal of ABA–induced stomatal closure by phenolic compounds. Journal of Experimental Botany, 37, 129–134.Google Scholar
  135. Reinders, A., Schulze, W., Kuhn, C., Barker, L., Schulz, A., Ward, J. M., et al. (2002). Protein–protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell, 14, 1567–1577.PubMedGoogle Scholar
  136. Rennie, E. A., & Turgeon, R. (2009). A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences of the United States of America, 106, 14162–14167.PubMedGoogle Scholar
  137. Roberts, A. G., & Oparka, K. J. (2003). Plasmodesmata and the control of symplasmic transport. Plant, Cell and Environment, 26, 103–124.Google Scholar
  138. Ruan, Y. L., & Patrick, J. W. (1995). The cellular pathway of postphloem sugar-transport in developing tomato fruit. Planta, 196, 434–444.Google Scholar
  139. Ruiz-Medrano, R., Xoconostle-Cazares, B., & Kragler, F. (2004). The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Current Opinion in Plant Biology, 7, 641–650.PubMedGoogle Scholar
  140. Russell, J. W., Golovoy, D., Vincent, A. M., Mahendru, P., Olzmann, J. A., Mentzer, A., et al. (2002). High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. The FASEB Journal, 16, 1738–1748.Google Scholar
  141. Sahar, K., Amin, B., & Taher, N. M. (2011). The salicylic acid effect on the Salvia officinalis L. sugar protein and prolin contents under salinity (NaCl) stress. Journal of Stress Physiology and Biochemistry, 7, 80–87.Google Scholar
  142. Samardakiewicz, S., Krzesłowska, M., Bilski, H., Bartosiewicz, R., & Woźny, A. (2012). Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma, 249, 347–351.PubMedGoogle Scholar
  143. Sauer, N. (2007). Molecular physiology of higher plant sucrose transporters. FEBS Letters, 581, 2309–2317.PubMedGoogle Scholar
  144. Scholthof, H. B. (2005). Plant virus transport: motions of functional equivalence. Trends in Plant Science, 10, 376–382.PubMedGoogle Scholar
  145. Schroeder, J. I., & Hagiwara, S. (1989). Cytosolic calcium regulates ion channels in plasma membrane of Vicia faba guard cells. Nature, 338, 427–430.Google Scholar
  146. Schulz, A. (2005) Role of plasmodesmata in solute loading and unloading. In: K. J. Oparka (Ed.) Plasmodesmata. Annual Plant Reviews (Vol. 18, pp. 135–161). Oxford: Blackwell Science.Google Scholar
  147. Serova, V. V., Raldugina, G. N., & Krasavina, M. S. (2006). Inhibition of callose hydrolysis by salicylic acid disturbs transport of tobacco mosaic virus. Doklady Biochemistry and Biophysics, 406, 36–39.PubMedGoogle Scholar
  148. Shah, J., & Klessig, D. F. (1996). Identification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related β-1,3-glucanase gene, PR-2d. The Plant Journal, 10, 1089–1101.PubMedGoogle Scholar
  149. Shaaban, M. M., Abd El-Aal A. M. K., & Ahmed, F. F. (2011). Insight into the effect of salicylic acid on apple trees growing under sandy saline. Soil Research Journal of Agricultural and Biological Science, 7, 150–156.Google Scholar
  150. Shakirova, F. M., Sakhabutdinova, D. R., Bezrukova, M. V., Fatkhutdinova, R. F., & Fatkhutdinova, D. R. (2003). Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science, 164, 317–322.Google Scholar
  151. Shehata, S. A. M., Ibrahim, S. I., & Zaghlool, S. A. M. (2001). Physiological response of flag leaf and ears of maize plant induced by foliar application of kinetin and acetyl salicylic acid. Annals of Agricultural Science, Ain Shams University Cairo, 46, 435–449.Google Scholar
  152. Shimoura, T., & Dijkstra, J. (1975). The occurrence of callose during the process of local lesion formation. Netherlands Journal of Plant Pathology, 81, 107–121.Google Scholar
  153. Siegel, R. S., Xue, S., Murata, Y., Yang, Y., Nishimura, N., Wang, A., et al. (2009). Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells. The Plant Journal, 59, 207–220.PubMedGoogle Scholar
  154. Simpson, C., Thomas, C., Findlay, K., Bayer, E., & Maule, A. J. (2009). An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell, 21, 581–594.PubMedGoogle Scholar
  155. Singh, B., & Usha, K. (2003). Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regulation, 39, 137–141.Google Scholar
  156. Sinha, S. K., Srivastava, H. S., & Tripathi, R. B. (1993). Influence of some growth regulators and cations on inhibition of chlorophyll biosynthesis by lead in Maize. Bulletin of Environmental Contamination and Toxicology, 51, 241–246.PubMedGoogle Scholar
  157. Slewinski, T. L., & Braun, D. M. (2010). Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Science, 178, 341–349.Google Scholar
  158. Sondergaard, T. E., Schulz, A., & Palmgren, M. G. (2004). Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiology, 136, 2475–2482.PubMedGoogle Scholar
  159. Srivastava, A. C., Ganesan, S., Ismail, I. O., & Ayre, B. G. (2008). Functional characterization of the Arabidopsis AtSUC2 sucrose/H+ symporter by tissue-specific complementation. Reveals an essential role in phloem loading but not in long-distance transport. Plant Physiology, 148, 200–211.PubMedGoogle Scholar
  160. Srivastava, A. C., Dasgupta, K., Ajieren, E., Costilla, G., McGarry, R. C., & Ayre, B. G. (2009). Arabidopsis plants harbouring a mutation in AtSUC2, encoding the predominant sucrose/proton symporter necessary for efficient phloem transport, are able to complete their life cycle and produce viable seed. Annals of Botany, 104, 1121–1128.PubMedGoogle Scholar
  161. Stadler, R., Lauterbach, C., & Sauer, N. (2005a). Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiology, 139, 701–712.PubMedGoogle Scholar
  162. Stadler, R., Wright, K. M., Lauterbach, C., Amon, G., Gahrtz, M., Feuerstein, A., et al. (2005b). Expression of GFP-fusions in Arabidopsis companion cells reveals nonspecific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. The Plant Journal, 41, 319–331.PubMedGoogle Scholar
  163. Stonebloom, S., Brunkard, J., Cheung, A., Jiang, K., Feldman, L., & Zambryski, P. (2012). Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiology, 158, 190–199.PubMedGoogle Scholar
  164. Stonebloom, S., Burch-Smith, T., Kim, I., Meinke, D., Mindrinos, M., & Zambryski, P. (2009). Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proceedings of the National Academy of Sciences of the United States of America, 106, 17229–17234.PubMedGoogle Scholar
  165. Summermatter, K., Sticher, L., & Metraux, J. P. (1995). Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae. Plant Physiology, 108, 1379-1385.Google Scholar
  166. Thompson, M. V. (2006). Phloem: The long and the short of it. Trends in Plant Science, 11, 26–32.PubMedGoogle Scholar
  167. Truernit, E., & Sauer, N. (1995). The promoter of the Arabidopsis thaliana SUC2 sucrose–H+ symporter gene directs expression of beta-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta, 196, 564–570.PubMedGoogle Scholar
  168. Turgeon, R., & Gowan, E. (1990). Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiology, 94, 1244–1249.PubMedGoogle Scholar
  169. Turgeon, R., & Medville, R. (2011). Amborella trichopoda, plasmodesmata, and the evolution of phloem loading. Protoplasma, 248, 173–180.PubMedGoogle Scholar
  170. Ueki, S., & Citovsky, V. (2011). To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Molecular Plant, 4, 782–793.PubMedGoogle Scholar
  171. Ueki, S., Spektor, R., Natale, D. M., & Citovsky, V. (2010). ANK, a host cytoplasmic receptor for the tobacco mosaic virus cell-to-cell movement protein, facilitates intercellular transport through plasmodesmata. PLoS Pathogens, 6, 1–13.Google Scholar
  172. Uzunova, A. N., & Popova, L. P. (2000). Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica, 38, 243–250.Google Scholar
  173. Van Bel, A. J. (2003a). The phloem, a miracle of ingenuity. Plant, Cell and Environment, 26, 125–149.Google Scholar
  174. Van Bel, A. J. (2003b). Transport phloem: Low profile, high impact. Plant Physiology, 131, 1509–1510.PubMedGoogle Scholar
  175. White, R.G., Badelt, K., Overall, R.L., & Vesk, M. (1994). Actin associated with plasmodesmata. Protoplasma, 180, 169–184.Google Scholar
  176. White, R. G., & Barton, D. A. (2011). The cytoskeleton in plasmodesmata: a role in intercellular transport? Journal of Experimental Botany, 62, 5249–5266.PubMedGoogle Scholar
  177. Wolff, S. P., & Dean, R. T. (1987). Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochemical Journal, 245, 243–250.PubMedGoogle Scholar
  178. Yarullina, L. G., Troshina, N. B., Cherepanova, E. A., Zaikina, E. A., & Maksimov, I. V. (2011). Salicylic and jasmonic acids in regulation of the proantooxidant state in wheat leaves infected by Septoria nodorum Berk. Applied Biochemistry and Microbiology, 47, 602–608.Google Scholar
  179. Zahra, S., Amin, B., Ali, M. V. S., Ali, Y., & Mehdi, Y. (2010). The salicylic acid effect on the tomato Lycopersicum esculentum Mill.) sugar, protein and proline contents under salinity stress (NaCl). Journal of Biophysics and Structural Biology, 2, 35–41.Google Scholar
  180. Zavaliev, R., Ueki, S., Epel, B. L., & Citovsky, V. (2011). Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma, 248, 117–130.PubMedGoogle Scholar
  181. Zeidne, G., Sadja, R., & Reuveny, E. (2001). Redox-dependent gating of G protein-coupled inwardly rectifying K+ channels. Journal of Biological Chemistry, 276, 35564–35570.Google Scholar
  182. Zhang, W.-H., Zhou, Y., Dibley, K. E., Tyerman, S. D., Furbank, R. T., & Patrick, J. W. (2007). Nutrient loading of developing seeds. Functional Plant Biology, 34, 314–331.Google Scholar
  183. Zhang, X.-Y., Wang, X.-L., Wang, X.-F., Xia, G.-H., Pan, Q.-H., Fan, R.-C., et al. (2006). A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiology, 142, 220–232.PubMedGoogle Scholar
  184. Zhen, X.-H., & Li, Y.-Z. (2004). Ultrastructural changes and location of ß-1,3-glucanase in resistant and susceptible cotton callus cells in response to treatment with toxin of Verticillium dahliae and salicylic acid. Journal of Plant Physiology, 161, 1367–1377.PubMedGoogle Scholar
  185. Zhao, H. J., Lin, X. W., Shi, H. Z., & Chang, S. M. (1995). The regulating effects of phenolic compounds on the physiological characteristics and yield of soybeans. Acta Agronomica Sinica, 21, 351–355.Google Scholar
  186. Zhou, Y., Qu, H., Dibley, K. E., Offler, C. E., & Patrick, J. W. (2007). A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators. The Plant Journal, 49, 750–764.PubMedGoogle Scholar
  187. Zippel, R., & Ehwald, R. (1980). Accumulation of 2-deoxy-d-glucose in the maize radicle after import via the phloem. Biochemie und Physiologie der Pflanzen, 175, 676–680.Google Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of ScienceMoscowRussia

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