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


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.



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




  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.

    CAS  PubMed  PubMed Central  Google 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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  Google Scholar 

  13. 13.

    Grattan, S. R., Grieve, C. M. (1999) Salinity-mineral nutrient relations in horticultural crops. Sci. Hort. 78, 127–157.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  Google Scholar 

  22. 22.

    Konieczynski, P., Wesolowski, M. (2007) Total phosphorus and its extractable form in plant drugs. Food Chem. 103, 210–216.

    CAS  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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  Google Scholar 

  27. 27.

    Mimura, T. (1999) Regulation of phosphate transport and homeostasis in plant cells. Int. Rev. Cytol. 191, 149–200.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  PubMed  PubMed Central  Google 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.

    CAS  Google Scholar 

  35. 35.

    Shenoy, V. V., Kalagudi, G. M. (2005) Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnol. Adv. 23, 501–513.

    CAS  PubMed  Google 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.

    CAS  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.

    CAS  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.

    CAS  PubMed  Google 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.

    CAS  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.

    CAS  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.

    CAS  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.

    CAS  PubMed  Google 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.

    CAS  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 

Download references

Author information



Corresponding author

Correspondence to Nehla Labidi.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), 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.

Reprints and Permissions

About this article

Cite this article

Labidi, N., Snoussi, S., Ammari, M. et al. Enhancement of Acid Phosphatase Secretion and PI Acquisition in Suaeda Fruticosa on Calcareous Soil by High Saline Level. BIOLOGIA FUTURA 61, 470–485 (2010). https://doi.org/10.1556/ABiol.61.2010.4.10

Download citation


  • Suaeda fruticosa
  • salinity
  • P acquisition acid
  • alkaline phosphatases activities