Acta Biologica Hungarica

, Volume 61, Issue 4, pp 470–485 | Cite as

Enhancement of Acid Phosphatase Secretion and PI Acquisition in Suaeda Fruticosa on Calcareous Soil by High Saline Level

  • Nehla LabidiEmail author
  • Sana Snoussi
  • Manel Ammari
  • Wissal Metoui
  • N. Ben Yousfi
  • Lamia Hamrouni
  • C. Abdelly


The aim of this study was to identify the relationship between the adaptive processes of Suaeda fruticosa for Pi acquisition and the physic-chemical and biological characteristics of two soil types under moderate and high saline conditions. Four treatments were established in pots: namely SS100, SS600, CS100 and CS600 where SS stood for sandy soil and CS for calcareous soil, and the indexes 100 and 600 were NaCl concentrations (mM) in irrigation distilled water. Assuming that Pi per g of plant biomass is an indicator of plant efficiency for P acquisition, the results showed that Pi acquisition was easiest on SS100 and was difficult on CS100. The differences in Pi acquisition between plants on SS100 and CS100 could be attributed to the low root surface area (−30%) and to the low alkaline phosphatases (Pases) activities (−50%) in calcareous rhizospheric soil. The high salinity level had no effect on the efficiency of P acquisition on SS but increased this parameter on CS (+50%). In the latter soil type, high acid phosphatase activities were observed in rhizospheric soil at high salinity level. Acid phosphatase seemed to be secreted from the roots. The higher secretion of acid phosphatase in this soil was related to the root lipid peroxidation in response to elevated salinity associated with the augmentation of unsaturated acids which might induce an oxidative damage of the root membrane. Thus we can conclude that in deficient soil such as calcareous, the efficiency of P acquisition in S. fruticosa which was difficult at moderate salinity level can be enhanced by high salinity level.


Suaeda fruticosa salinity P acquisition acid alkaline phosphatases activities 



dry weight


fresh weight


electric conductivity


inorganic phosphorus


sandy soil


calcareous soil


scanning electron microscopy




stomatal density


guard cell length


stomatal pore area


Net photosynthetic rate


leaf surface area

ch a

chlorophyll a

ch b

chlorophyll b




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Allen, C., Good, P. (1971) Acyl lipids in photosynthetic systems. In: Colowic, S. P., Kaplan, N. O. (eds) Methods in Enzymology. Academic Press, New York, pp. 523–547.Google Scholar
  2. 2.
    Arnon, D. I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant. Physiol. 24, 1–5.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Besford, R. T. (1979) Phosphorus nutrition and acid phosphatase activity in leaves of seven plant species. J. Sci. Food Agr. 30, 282–285.Google Scholar
  4. 4.
    Bollons, H. M., Barraclough, P. B. (1997) Inorganic orthophosphate for diagnosing the phosphorus status of wheat plants. J. Plant. Nutr. 20, 641–655.Google Scholar
  5. 5.
    Dinkelaker, B., Römheld, V., Marschner, H. (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant. Cell. Environ. 12, 285–292.Google Scholar
  6. 6.
    Drouineau, G. (1942) Dosage rapide du calcaire actif du sol: Nouvelles données sur la separation et la nature des fractions calcaires. Annales Agronomiques 12, 441–450.Google Scholar
  7. 7.
    Duff, R. B., Webley, D. M., Scott, R. O. (1967) Solubilization of minerals and related materials by 2-ketogluconic acid producing bacteria. Soil. Sci. 5, 105–114.Google Scholar
  8. 8.
    El-Tarabily., Khaled, A., Nassar, A. H., Sivasithamparam, K. (2008) Promotion of growth of bean (Phaseolus vulgaris L.) in a calcareous soil by a phosphate-solubilizing, rhizosphere-competent isolate of Micromonospora endolithica. App. Soil Ecol. 39, 161–171.Google Scholar
  9. 9.
    Fleury, P., Leclerc, M. (1943) La méthode nitro-vanadomolybdique de mission pour le dosage colo-rimétrique du phosphore. Son intérêt en biochimie. Bull. Chim. Biol. 25, 201–205.Google Scholar
  10. 10.
    Fu, X., Shao, M., Wei, X., Horton, R. (2009) Effects of two perennials, fallow and millet on distribution of phosphorous in soil and biomass on sloping loess land, China. Catena 77, 200–206.Google Scholar
  11. 11.
    Gee, G. W., Bauder, J. W. (1986) Particle-size analysis. In: Black, W. C. (ed.) Methods of Soil Analysis. Part 1. American Society of Agronomy, Madison, Wisconsin, pp. 398–406.Google Scholar
  12. 12.
    George, T. S., Turner, B. L., Gregory, P. J., Cade-Menun, B. J., Richardson, A. E. (2006) Depletion of organic phosphorus from oxisols in relation to phosphatase activities in the rhizosphere. Eur. J. Soil Sci. 57, 47–57.Google Scholar
  13. 13.
    Grattan, S. R., Grieve, C. M. (1999) Salinity-mineral nutrient relations in horticultural crops. Sci. Hort. 78, 127–157.Google Scholar
  14. 14.
    Grime, J. P. (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169–1194.Google Scholar
  15. 15.
    Halajnia, A., Haghnia, G. H., Fotovat, A., Khorasani, R. (2009) Phosphorus fractions in calcareous soils amended with P fertilizer and cattle manure. Geoderma 150, 209–213.Google Scholar
  16. 16.
    Halvorson, H. O., Keynan, A., Kornberg, H. L. (1990) Utilization of calcium phosphates for microbial growth at alkaline pH. Soil Biol. Biochem. 22, 887–890.Google Scholar
  17. 17.
    Henry, A., Chaves, N. F., Kleinman, P. J. A., Lynch, J. P. (2010) Will nutrient-efficient genotypes mine the soil? Effects of genetic differences in root architecture in common bean (Phaseolus vulgaris L.) on soil phosphorus depletion in a low-input agro-ecosystem in Central America. Field. Crop. Res. 115, 67–78.Google Scholar
  18. 18.
    Hrynkiewicz, K., Baum, C., Leinweber, P. (2009) Mycorrhizal community structure, microbial biomass P and phosphatase activities under Salix polaris as influenced by nutrient availability. Eur. J. Soil. Biol. 45, 168–175.Google Scholar
  19. 19.
    Hysek, J., B. Sarapatka, B. (1998) Relationship between phosphatase active bacteria and phosphatase activities in forest soils. Biol. Fertil. Soils 26, 112–115.Google Scholar
  20. 20.
    Juma, N. G., Tabatabai, M. A. (1988) Phosphatase activity in corn and soybean roots: conditions for assay and effects of metals. Plant Soil 107, 30–47.Google Scholar
  21. 21.
    Kelleher, B. P., Willeford, K. O., Simpson, A. J., Simpson, M. J., Stout, R., Rafferty, A., Kingery, W. L. (2004) Acid phosphatase interactions with organo-mineral complexes: influence on catalytic activity. Biogeochemistry 71, 285–297.Google Scholar
  22. 22.
    Konieczynski, P., Wesolowski, M. (2007) Total phosphorus and its extractable form in plant drugs. Food Chem. 103, 210–216.Google Scholar
  23. 23.
    Loussert, R., Brousse, G. (1978) L’olivier. Editions Maisonneuve et Larose, pp. 167–175.Google Scholar
  24. 24.
    Lung, S. C., Leung, A., Kuang, R., Wang, Y., Leung, P., Lim, B. L. (2008) Phytase activity in tobacco (Nicotiana tabacum) root exudates is exhibited by a purple acid phosphatase. Phytochemistry 69, 365–373.PubMedGoogle Scholar
  25. 25.
    Ma, X. F, Wright, E., Ge, Y., Bell, J., Xi, Y, Bouton, J. H, Wang, Z. Y (2009) Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant. Sci. 176, 479–488.PubMedGoogle Scholar
  26. 26.
    Marschner, P., Solaiman, Z., Rengel, Z. (2005) Growth, phosphorus uptake and rhizosphere microbial community composition of a phosphorus-efficient wheat cultivar in soils differing in pH. J. Plant. Nutr. Soil. Sci. 168, 343–351.Google Scholar
  27. 27.
    Mimura, T. (1999) Regulation of phosphate transport and homeostasis in plant cells. Int. Rev. Cytol. 191, 149–200.Google Scholar
  28. 28.
    Naidoo, G. (2009) Differential effects of nitrogen and phosphorus enrichment on growth of dwarf Avicennia marina mangroves. Aqua. Bot. 90, 184–190.Google Scholar
  29. 29.
    Olsen, S. R., Cole, C. V., Watanabe, F. S., Dean, L. A. (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Dep. Agric. Circ. 939, 1–19.Google Scholar
  30. 30.
    Parkinson, D., Gray, T. R. G., Williams, S. T. (1971) Methods for studying the ecology of soil microorganisms. IBP Handbook 19. Blackwell, p. 108.Google Scholar
  31. 31.
    Raiesi, F., Ghollarata, M. (2006) Interactions between phosphorus availability and an AM fungus (Glomus intraradices) and their effects on soil microbial respiration, biomass and enzyme activities in a calcareous soil. Pedobiologia 50, 413–425.Google Scholar
  32. 32.
    Ruiz, J. M., Belakbir, A., Romero, L. (1996) Foliar level of phosphorus and its bioindicators in Cucumis melo grafted plants. A possible effect of rootstock. J. Plant. Physiol. 149, 400–404.Google Scholar
  33. 33.
    Schachtman, D. P., Robert, J. R., Ayling, S. M. (1998) Phosphorus uptake by plants: from soil to cell. Plant physiol. 116, 447–453.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Schmedes, A., Holmer, G. (1989) Anew thiobarbituric acid(TBA) method for determinig free malon-dialdehyde (MDA) and hydroproxides selectively as a measure of lipid peroxidations. JAOCS 66, 813–817.Google Scholar
  35. 35.
    Shenoy, V. V., Kalagudi, G. M. (2005) Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnol. Adv. 23, 501–513.PubMedGoogle Scholar
  36. 36.
    Skujins, J. J., Braal, L., McLaren, A. D. (1962) Characterization of phosphatase in a terrestial soil sterilized with an electron beam. Enzyme 25, 125–133.Google Scholar
  37. 37.
    Su, J. Y, Zheng, Q., Li, H. W., Li, B., Jing, R. L., Tong, Y. P., Li, Z. S. (2009) Detection of QTLs for phosphorus use efficiency in relation to agronomic performance of wheat grown under phosphorus sufficient and limited conditions. Plant. Sci. 176, 824–836.Google Scholar
  38. 38.
    Szekely, Gy., Abraham, E., Cseplo, A., Rigo, G., Zsigmond, L., Csiszar, J., Ayaydin, F., Strizhov, N., Jasik, J., Schmelzer, E., Koncz, Cs., Szabados, L. (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53, 11–28.PubMedGoogle Scholar
  39. 39.
    Tabatabai, M. A. (1982) Soil enzymes. In: Methods of Soil Analysis. Part 2. Agronomy Monograph 9. ASA-SSSA, Madison, Wisconsin, pp. 903–947.Google Scholar
  40. 40.
    Tang, C., Han, X. Z., Qiao, Y. F., Zheng, S. J. (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environ. Exp. Bot. 67, 228–234.Google Scholar
  41. 41.
    Tarafdar, J. C., Ciaassen, N. (2005) Preferential utilization of organic and inorganic sources of phosphorus by wheat plant. Plant Soil 275, 285–293.Google Scholar
  42. 42.
    Torrecillas, A., Leon, A., F. Del Amor, F., Martinez-Monpean, M. C. (1984) Determinacion rapida de clorofila en discos foliares de limonero. Fruits 39, 617–622.Google Scholar
  43. 43.
    Touchette, B. W., Burkholder, J. M. (2000) Review of nitrogen and phosphorus metabolism in sea-grasses. J. Exp. Mar. Biol. Ecol. 250, 133–167.PubMedGoogle Scholar
  44. 44.
    Walkley, A., Black, I. A. (1934) An examination of Degtjareff method for determination soil organic matter and a proposed modification of the chromic acid titration method. Soil. Sci. 37, 29–37.Google Scholar
  45. 45.
    Wissuwa, M. (2003) How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiol. 133, 1–12.Google 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
  • Sana Snoussi
    • 1
  • Manel Ammari
    • 1
  • Wissal Metoui
    • 1
  • N. Ben Yousfi
    • 1
  • Lamia Hamrouni
    • 1
  • C. Abdelly
    • 1
  1. 1.Laboratoire d’Adaptation des Plantes aux Stress AbiotiquesCentre de Biotechnologie, Technopole de Borj CédriaHammam-LifTunisie

Personalised recommendations