Acta Biologica Hungarica

, Volume 61, Issue 3, pp 299–312 | Cite as

Salt Excretion in Suaeda Fruticosa

  • Nehla LabidiEmail author
  • Manel Ammari
  • Dorsaf Mssedi
  • Maali Benzerti
  • Sana Snoussi
  • C. Abdelly


Suaeda fruticosa is a perennial “includer” halophyte devoid of glands or trichomes with a strong ability of accumulating and sequestrating Na+ and Cl-. We were interested in determining whether leaf cuticle salt excretion could be involved as a further mechanism in salt response of this species after long-term treatment with high salinity levels. Seedlings had been treated for three months with seawater (SW) diluted with tap water (0, 25, 50 and 75% SW). Leaf scanning electron microscopy revealed a convex adaxial side sculpture and a higher accumulation of saline crystals at the lamina margin, with a large variability on repartition and size between treatments. No salt gland or salt bladder was found. Three-dimensional wax decorations were the only structures found on leaf surface. Washing the leaf surface with water indicated that sodium and chloride predominated in excreted salts, and that potassium was poorly represented. Optimal growth of whole plant was recorded at 25% SW, correlating with maximum Na+ and Cl- absolute secretion rate. The leaves of plants treated with SW retained more water than those of plants treated with tap water due to lower solute potential, especially at 25% SW. Analysis of compatible solute, such as proline, total soluble carbohydrates and glycinebetaine disclosed strong relationship between glycinebetaine and osmotic potential (r = 0.92) suggesting that tissue hydration was partly maintained by glycinebetaine accumulation. Thus in S. fruticosa, increased solute accumulation associated with water retention, and steady intracellular ion homeostasis confirms the “includer” strategy of salt tolerance previously demonstrated. However, salt excretion at leaf surface also participated in conferring to this species a capacity in high salinity tolerance.


Halophyte includer strategy excluder strategy proline glycinebetaine salt excretion 



dry weight


electric conductivity




leaf osmotic potential


scanning electron microscopy




total soluble carbohydrates


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bates, L. S., Waldren, R. P., Teare I. D. (1973) Rapid determination of free proline for water stress studies. Plant Soil 39, 205–207.CrossRefGoogle Scholar
  2. 2.
    Benwahhoud, M., Jouad, H., Eddouks, M., Lyoussi, B. (2001) Hypoglycemic effect of Suaeda fruti-cosa in streptozotocin induced diabetic rats. J. Ethnopharm. 76, 35–38.CrossRefGoogle Scholar
  3. 3.
    Boucaud, J., Ungar I. A. (1978) Halophile et resistance au sel dans le genre Suaeda Forssk. Bulletin de la Société Botanique de France, Actualité Botanique 34, 23–35.CrossRefGoogle Scholar
  4. 4.
    Brewer, C. A., Smith, W. K., Vogelmann T. C. (1991) Functional interaction between leaf trichomes, leaf wettability and the optical properties of water droplets. Plant Cell Environ. 14, 955–962.CrossRefGoogle Scholar
  5. 5.
    Buchholz, A., Schönherr, J. (2000) Thermodynamic analysis of diffusion of non electrolytes across plant cuticles in the presence and absence of the plasticiser tributyl phosphate. Planta 212, 103–111.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Chamel, A., Pineri, M., Escoubes, M. (1991) Quantitative determination of water sorption by plant cuticles. Plant Cell Environ. 14, 87–95.CrossRefGoogle Scholar
  7. 7.
    Clipson, N. J. W., Flowers T. J. (1987) Salt tolerance in the halophyte suaeda maritima (1.) dum. The effect of salinity on the concentration of sodium in the xylem. New Phytol. 105, 359–366.CrossRefGoogle Scholar
  8. 8.
    Connor, D. J. (1969) Growth of the grey mangrove Avicennia marina in nutrient culture. Biotropica 1, 36–40.CrossRefGoogle Scholar
  9. 9.
    Debez, A., Koyro, H. W., Grignon, C., Abdelly, C., Huchzermeyer, B. (2008) Relationship between the photosynthetic activity and the performance of Cakile maritima after long-term salt treatment. Physiol. Plant. 133, 373–385.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Debez, A., Saadaoui, D., Ramani, B., Ouerghi, Z., Koyro, H. W., Huchzermeyer, B., Abdelly, C. (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ. Exp. Bot. 57, 285–295.CrossRefGoogle Scholar
  11. 11.
    Drennan, P., Pammenter N. W. (1982) Physiology of salt secretion in the mangrove Avicennia marina (Forsk.) Vierh. New Phytol. 91, 597–606.CrossRefGoogle Scholar
  12. 12.
    Gale, J., Zeroni, M. (1984) Cultivation of plants in brackish water incontrolled environmental agriculture. In: Staples, R. C., Toenniessen G. R. (eds) Salinity Tolerance inPlants. John Wiley and Sons, New York, 363–380.Google Scholar
  13. 13.
    Grieve, C. M., Grattan S. R. (1983) Rapid assay for determination of water-soluble quaternary ammonium-compounds. Plant Soil 70, 303–307.CrossRefGoogle Scholar
  14. 14.
    Hameed, M., Ashraf, M. (2008) Physiological and biochemical adaptations of Cynodon dactylon (L.) Pers. from the Salt Range (Pakistan) to salinity stress. Flora 203, 683–694.CrossRefGoogle Scholar
  15. 15.
    Hewitt, E. J. (1966) Sand and water culture methods used in the study of plant nutrition. Commonw. Agr. Bur. Tech. Commun. 22. (revised 2nd ed.).Google Scholar
  16. 16.
    Hoagland, D. R., Anion D. R. (1950) Growing plants without soil by the water-culture method. Calif. Agric. Exp. Sta. Cir. 347, 1–32.Google Scholar
  17. 17.
    Hong-Bo, S., Li-Ye, C., Ming-An, S., Shi-Qing, L., Ji-Cheng, Y (2008) Bioengineering plant resistance to abiotic stresses by the global calcium signal system. Biotechnol. Adv. 26, 503–510.PubMedCrossRefGoogle Scholar
  18. 18.
    Jacobson, L. (1951) Maintenance of iron supply in nutrient solutions by a single addition of ferric-potassium-ethylene-diamine-tetraacetate. Plant Physiol. 26, 411–413.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Kefu, Z., Hai, F., Harris P. J. C. (1995) The physiological basis of growth inhibition of halophytes by potassium. In: Khan, M. A., Ungar I. A. (eds) Biology of Salt Tolerant Plants. Department of Botany, University of Karachi, Karachi, pp. 221–227.Google Scholar
  20. 20.
    Khan, M. A., Ungar, I. A., Showalter A. M. (2000) The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. J. Arid Environ. 45, 73–84.CrossRefGoogle Scholar
  21. 21.
    Kirst, G. O. (1989) Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 21–53.Google Scholar
  22. 22.
    Kleber, H. P., Schlee, D., Schöpp, W. (1987) Biochemisches Praktikum. 2. Aufl. G. Fischer, Jena.Google Scholar
  23. 23.
    Koch, K., Bhushan, B., Barthlott, W. (2009) Multifunctional surface structures of plants: An inspiration for biomimetics. Prog. Mater. Sci. 54, 137–178.CrossRefGoogle Scholar
  24. 24.
    Koch, K., Ensikat H. J. (2008) The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron 39, 759–772.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Koyro, H.-W., Geissler, N., Hussin, S. (2009) Survival at Extreme Locations: Life Strategies of Halophytes. Salinity and Water Stress 44, 167–177.CrossRefGoogle Scholar
  26. 26.
    Lefèvre, L., Marchai, G., Meerts, P., Corréal, E., Lutts, S. (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ. Exp. Bot. 65, 142–152.CrossRefGoogle Scholar
  27. 27.
    Mahmood, K., Malik, K. A., Lodhi M. A. K., Sheikh K. H. (1996) Seed germination and salinity tolerance in plant species growing on saline wetlands. Biol. Plant. 38, 309–315.CrossRefGoogle Scholar
  28. 28.
    Masuko, T., Minami, A., Iwasaki, N., Majima, T., Nishimura, S.-I., Lee Y. C. (2005) Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal. Biochem. 339, 69–72.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Naidoo, G., Somara, R., Achar, P. (2008) Morphological and physiological responses of the halo-phyte, Odyssea paucinervis (Staph) (Poaceae), to salinity. Flora 203, 437–447.CrossRefGoogle Scholar
  30. 30.
    Neinhuis, C., Barthlott, W. (1997) Characterization and distribution of water-repellent, self-cleaning plant surfaces. Ann. Bot. 79, 667–677.CrossRefGoogle Scholar
  31. 31.
    Popp, C., Burghardt, M., Friedmann, A., Riederer, M. (2005) Characterization of hydrophilic and lipophilic pathways of Hedera helix L. cuticular membranes: permeation of water and uncharged organic compounds. J. Exp. Bot. 56, 2797–2806.PubMedCrossRefGoogle Scholar
  32. 32.
    Qiu, N., Chen, M., Guo, J., Bao, H., Ma, X., Wang, B. (2007) Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa. Plant Sci. 172, 1218–1225.CrossRefGoogle Scholar
  33. 33.
    Rabhi, M., Hafsi, C., Lakhdar, A., Hajji, S., Barhoumi, Z., Hamrouni, M. H., Abdelly, C., Smaoui, A. (2009) Evaluation of the capacity of three halophytes to desalinize their rhizosphere as grown on saline soils under nonleaching conditions. Afr. J. Ecol. 47, 463–468.CrossRefGoogle Scholar
  34. 34.
    Ravindran, K. C., Venkatesan, K., Balakrishnan, V., Chellappan, K. P., Balasubramanian, T. (2007) Restoration of saline land by halophytes for Indian soils. Soil Biol. Biochem. 39, 2661–2664.CrossRefGoogle Scholar
  35. 35.
    Riederer, M., Schreiber, L. (1995) Waxes-the transport barriers of plant cuticles. In: Hamilton, R. J. (ed.) Waxes: Chemistry, Molecular Biology and Functions. The Oily Press, Dundee, Scotland, pp. 131–156.Google Scholar
  36. 36.
    Rozema, J., Gude, H., Pollak, G. (1981) An ecophysiological study of the salt secretion of four halophytes. New Phytol. 89, 201–217.CrossRefGoogle Scholar
  37. 37.
    Scholander, P. F., Hammel, H. T., Bradstreet, E. D., Hemmingsen E. A. (1965) Sap pressure in vascular plants. Science 148, 339–346.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Schönherr, J. (2002) A mechanistic analysis of penetration of glyphosate salts across astomatous cuticular membranes. Pest Manage. Sci. 58, 343–351.CrossRefGoogle Scholar
  39. 39.
    Schönherr, J. (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J. Exp. Bot. 57, 2471–2491.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Shi-qing, L. I., Chun-rong, J. I., Ya-ning, F., Xiao-li, C., Sheng-xiu, L. I. (2008) Advances in nitrogen loss leached by precipitation from plant canopy. Agric. Sci. China 7, 480–486.CrossRefGoogle Scholar
  41. 41.
    Sleimi, N., Abdelly, C. (2003) Salt tolerance strategy of two fodder halophytes species: Spartina alterniflora and Suaeda fruticosa. In: Lieth, H., Mochtchenko, M. (eds) Cash Crop Halophytes: Recent Studies. Kluwer Academic Publishers, pp. 79–86.CrossRefGoogle Scholar
  42. 42.
    Spiro, R. G. (1966) Characterization of carbohydrate units of glycoproteins. In: Colowick, S. P., Kaplan N. O. (eds) Methods in Enzymology 8. London & New York: Academic Press, pp. 26–52.Google Scholar
  43. 43.
    Szepesi, A., Csiszár, J., Gémes, K., Horváth, E., Horváth, F., Simon, M. L., Tari, I. (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and absci-sic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. J. Plant Physiol. 51, 145–150.Google Scholar
  44. 44.
    Weber, D. J., Ansari, R., Gul, B., Khan M. A. (2007) Potential of halophytes as source of edible oil. J. Arid Environ. 68, 315–321.CrossRefGoogle Scholar
  45. 45.
    Yang, C., Shi, D., Wang, D. (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge). Plant Growth Regul. 56, 179–190.CrossRefGoogle Scholar
  46. 46.
    Ye, C. J., Zhao K. F. (2003) Osmotically active compounds and their localization in the marine halophyte eelgrass. Biol. Plant 46, 137–140.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2010

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Nehla Labidi
    • 1
    Email author
  • Manel Ammari
    • 1
  • Dorsaf Mssedi
    • 1
  • Maali Benzerti
    • 1
  • Sana Snoussi
    • 1
  • C. Abdelly
    • 1
  1. 1.The Laboratory of Plant Adaptation to Abiotic Stress (LAPSA)Biotechnology Center at the Technopark of Borj-Cedria (CBBC)Hammam-LifTunisia

Personalised recommendations