Skip to main content

Effect of Solution Phosphorus Concentration on the Exudation of Oxalate Ions by Wheat (Triticum aestivum L.)

Abstract

A solution culture experiment was conducted to investigate the effect of solution phosphorus concentration on the exudation of citrate and oxalate ions by five different varieties of the wheat (Triticum aestivum L). Wheat varieties were grown in a modified Hoagland nutrient solution containing five phosphorus levels (0, 0.2, 0.3, 0.4 and 0.5 μg/mL). Increasing the concentration of P significantly decreased oxalic acid exuded from roots. The exudation of oxalic acid was maximum at 10 days time interval. All the varieties of wheat were equally effective in exudating oxalic acid. The time interval had no significant effect on P concentration in plants. But significant interactive effect on plant P was found between varieties and different time intervals.

Graphical Abstract

Five levels of solution phosphorus (0, 0.2, 0.3, 0.4, 0.5 µg/mL) affected the oxalic acid secretion in wheat crop. The concentration of oxalic acid decreased with the increased levels of phosphorus concentration. In phosphorus stress condition wheat seedling secreted higher amount of oxalic acid.

Introduction

Phosphorus is one of the essential nutrients for plant growth and crop production. The importance of phosphorus in maintaining soil fertility and improving crop productivity has now been recognized much more than before in view of the fact that about 66 % of Indian soils are known to give universal response to P application and remaining 34 % to heavy feeding crops [1]. Phosphorus deficiency is a limiting factor of crop production in agricultural soils worldwide [24]. Correcting P deficiency with application of P fertilizers is not possible for the resource-poor farmers in the tropics and subtropics, especially on soil with high P fixing capacity. Knowledge about the principle mechanisms involved in efficient P acquisition by plants increased substantially during recent years [5, 6]. It has been attempted to use organic acids like citric acid and oxalic acid to extract labile P as an indicator of soil P availability [7, 8]. Low-molecular-weight oxalic acid plays an important role in the mobilization of soil phosphorus [9]. Oxalic acid exudation from roots is considered to be one of the mechanisms for plants to adapt to P deficiency [10] by mobilizing P in soil. The objective of the present study was to investigate the effect of solution phosphorus on the exudation of oxalic acid, in different varieties of wheat at different time intervals in sand culture.

Material and Methods

Seeds of different potential yield and genetic characters of wheat varieties viz. HD 2687; HD 2733; HD 2643, HD 2932; HD 2894 (Table 1) obtained from division of genetics, IARI, New Delhi were germinated on moist blotting paper in petriplates. After 7 days, the seedlings were taken out from petriplates and washed carefully under tap water to remove the adhering particles. Three seedlings of uniform size were selected and transplanted in PVC pots (3 cm diameter × 7 cm high) containing sand and graded doses of P (P1 = 0.0, P2 = 0.2, P3 = 0.3, P4 = 0.4 and P5 = 0.5 μg/mL) with Hoagland solution. Solution from the pots was collected through outlet by displacement method intermittently at 5, 10, 20 and 30 days after transplanting and stored in refrigerator and then analyzed for citrate and oxalate ions with HPLC (Water 600 controller as a Water’s USA) using a PDA detector. At each time interval, plants were harvested, oven dried at 70 °C and analyzed for P concentration by yellow color method [11]. Statistical analysis was done for factorial Complete Randomized Design [12]. During the experiment temperature was maintained between 21.5 and 39.8 °C and relative humidity between 51 and 90 %.

Table 1 Potential yield and genetic characters of the varieties

Results and Discussion

Oxalic and Citric Acids

The data on the organic acids revealed that wheat varieties exuded only oxalic acid. No citric acid was exuded. The concentration of oxalic acid decreased with the increasing level of phosphorus. P1 recorded the highest concentration of oxalic acid (1.88 μg/mL) and was followed by P2 (1.56 μg/mL), P3 (1.33 μg/mL), P4 (1.24 μg/mL) and P5 (1.20 μg/mL). The varieties did not show any significant effect on exudation of oxalic acid but, their interactive effect with levels of phosphorus concentration was significant (Table 2). It was maximum (2.79 μg/mL) in case of P1 (0 μg/mL) treatment with variety HD 2932 and minimum (0.84 μg/mL) in P4 (0.4 μg/mL) with variety HD 2733.

Table 2 Effect of P concentration in solution and different varieties on oxalic acid (μg/mL) exudation during sand culture

It is known that low molecular oxalic acid is secreted from plant roots in P deficient soil conditions and it is one of the mechanisms for plants to adapt to P deficiency [13]. Several studies have suggested that the exudation of organic acids by plant roots might be a physiological adaptation rather than a passive response of plants to P deficiency [14]. It has been postulated that increased exudation was due to increased membrane permeability induced by decrease in phospholipids in P deficient roots [15]. If this is true, then greater the degree of P starvation, the greater the amount of root exuded organic acids that would be expected. The addition of inorganic P to starved roots results in both depolarization of the plasma membrane and acidification of the cytoplasm by secretion of low molecular organic acids [16]. Present results have confirmed this hypothesis. Addition of P to the nutrient solution significantly decreased the exudation of oxalic acid. The exudation of oxalic acid was maximum (1.59 μg/mL) at 10 days time interval, followed by 20 days time interval, while the least concentration (1.15 μg/mL) was measured at 30 days time interval. The interactions between levels of phosphorus in solution and time interval were not significant (Table 3). Between 10 and 25 days after germination of wheat crop, root and shoot growth accelerated secretion of more amounts of organic substances, which enhanced microbial activity releasing more amount of photosynthate in the soil through roots [17]. It is largely accepted that up to 20–30 % of total C assimilated by higher plants is released in the rhizosphere as diverse exudates including respired CO2 [18].

Table 3 Effect of P concentration in solution and time interval on oxalic acid (μg/mL) exudation during sand culture

Phosphorus Concentration in Plants

The concentration of P in plant tissue increased with increased level of applied P (Table 4). In case of P1, it was 0.157 % while in case of P5, was 0.169 %. Different time interval had no significant effect on P concentration in plants, while the interaction effect between phosphorus concentration and time intervals was significant. The concentration of P was maximum (0.204 %) at 5 days time interval in the treatment P4 while it was minimum (0.105 %) at 5 days time interval in P3 (0.3 μg/mL). Increasing phosphorus concentration in soil solution enhanced the P uptake in crop plants. It might be due to more availability of labile phosphorus in soil solution [19]. More addition of inorganic P fertilizers at the period of vigorous growth of crop plant, directly enhanced the nutrient concentration in plant [20]. The concentration of P in different varieties was significant (Table 5). The lowest concentration was found in case of HD 2687 as 0.139 % while, highest in case of HD 2894 as 0.166 %. The interaction between phosphorus levels and varieties was also significant. The concentration of plant P was highest (0.193 %) in variety HD 2643 in P4, whereas lowest concentration (0.103 %) was seen in variety HD 2733 in P2 treatment. Phosphorus uptake by different varieties is affected by genetic potential of the varieties [21] as well as concentration of phosphorus in solution [20]. Transfer of inorganic P from the solution to the plant [22] involves a different set of thermodynamic parameters to those applying to the plasma membrane, mainly because of the millimolar concentrations in the cytoplasm and vacuoles [23]. The interaction between varieties and time interval was also found significant (Table 6). Maximum P-concentration (0.197 %) was recorded after 10 days time interval and minimum (0.129 %) after 30 days time interval in variety HD 2894. Different varieties having different genetic potential and biochemical reaction respond to particular ions from soil solution. In the present experiment, plant P concentration was improved substantially by the addition of P to the nutrient solution. This is due to the fact that increase in P concentration in solution near the root surface, increases P uptake rate in accordance with Michaelis and Menten equation [24]. Application of P is beneficial to the growth of wheat plant both in the field as well as under glasshouse condition. Exudation of oxalic acid plays an important role in the mobilization of soil phosphorus and ultimately enhances the concentration of P in plants [9].

Table 4 Effect of P concentration in solution and time interval on plant P concentration (%) during sand culture
Table 5 Effect of P concentration in solution and different varieties on plant P concentration (%) in sand culture
Table 6 Effect of varieties and time interval on P concentration (%) during sand culture

In conclusion, the present results suggest that the organic acid exudation from wheat crop roots follow the thumb rule of organic acid exudation under P stress conditions. It will be better if one identifies maximum exudation of oxalic acid at various time intervals and high organic acid exudation varieties in different crops, before applying P fertilizers accordingly. It will help to reduce the amount of P fertilizers application and secure the global food security.

References

  1. 1.

    Ganeshamurthy AN, Manjaiaha KM, Subba Rao A (1998) Mobilization of nutrients in tropical soils through worm casting: availability of macronutrients. Soil Biol Biochem 30(13):1671–1676

    Article  CAS  Google Scholar 

  2. 2.

    Schneider KD, Van Straaten P, Mira de Orduña R, Glasauer S, Trevors J, Fallow S, Smith PS (2010) Comparing phosphorus mobilization strategies using Aspergillus niger for the mineral dissolution of three phosphate rocks. J Appl Microbiol 108:366–374

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Luduena L, Pena D, Inanez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

    Article  CAS  Google Scholar 

  4. 4.

    Zhao X, Liu X, Guo C, Gu J, Xiao K (2012) Identification & characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol. doi:10.1007/s13562-012-0117-2

  5. 5.

    Raghothama KG (1999) Phosphate acquisition. Ann Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  CAS  Google Scholar 

  6. 6.

    Vashista P, Chaudhary N, Sharma CB (2006) Plant protein tyrosine phosphatases: an overview. Proc Natl Acad Sci, India Sect, B Biol Sci 76(3):207–215

    CAS  Google Scholar 

  7. 7.

    Wang Y, He Y, Zhang H, Schroder J, Li C, Zhou D (2008) Phosphate mobilization by citric, tartaric and oxalic acids in a clay loam Ultisol. Soil Sci Soc Am J 72:1263–1268

    Article  CAS  Google Scholar 

  8. 8.

    Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of phosphatases activity. Soil Bio Biochem 1:301–307

    Article  CAS  Google Scholar 

  9. 9.

    Wei LL, Chen CR, Xu ZH (2009) The effect of low-molecular-weight organic acids and in organic phosphorus concentration on the determination of soil phosphorus by the molybdenum blue reaction. Biol Fertil Soils 45:775–779

    Article  CAS  Google Scholar 

  10. 10.

    McDowell RW, Condron LM, Stewart I (2008) An examination of potential extraction methods to assess plant-available organic phosphorus in soil. Biol Fertil Soils 44:707–716

    Article  CAS  Google Scholar 

  11. 11.

    Jackson ML (1967) Soil chemical analysis. Prentice Hall of India Pvt. Ltd., New Delhi, pp 186–196

    Google Scholar 

  12. 12.

    Gomez KA, Gomez A (1983) Statistical procedures for agricultural research, 2nd edn. John Wiley & sons Inc, New York

    Google Scholar 

  13. 13.

    Jones DI, Darrah PR (1994) Role of root derived organic acids in mobilization of nutrients from rhizosphere. Plant Soil 166:247–257

    Article  CAS  Google Scholar 

  14. 14.

    Ohwaki Y, Hirata II (1992) Difference in carboxylic acid exudation among P- starved leguminous crops in relation to carboxylic acids contents in plant tissues and phospholipid level in roots. Soil Sci Plant Nutri 38(2):235–243

    Article  CAS  Google Scholar 

  15. 15.

    Graham JH, Leonard R, Menge JA (1981) Membrane mediated decrease in root exudation responsible for phosphorus inhibition of vasicular arbuscular mycorrhiza formation. Plant Physiol 68:548–552

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Ullrich-Eberius C, Novacky A, van Bel A (1984) Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta 161:46–52

    Article  CAS  Google Scholar 

  17. 17.

    Ishikawa S, Adu-Gyamfi JJ, Nakamura T, Yoshihara T, Watanabe T, Wagatsuma T (2002) Genotypic variability in phosphorus solubilizing activity of root exudates by pigeonpea grown in low-nutrient environments. Plant Soil 245(1):71–81

    Article  CAS  Google Scholar 

  18. 18.

    Helal HM, Sauerbeck D (1989) Carbon turnover in the rhizosphere. Z Pflanzenern Bodenk 152:211–216

    Article  CAS  Google Scholar 

  19. 19.

    Reddy DD, Rao AS, Rupa TR (2000) Effects of continuous use cattle manure and fertilizer phosphorus on crop yields and soil organic phosphorus in a vertisol. Biores Technol 75(2):113–118

    Article  CAS  Google Scholar 

  20. 20.

    Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  21. 21.

    Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Smeck NE (1985) Phosphorus dynamics in soil and landscapes. Geoderma 36(3–4):185–199

    Article  CAS  Google Scholar 

  23. 23.

    Lu YP, Zhen RG, Rea PA (1997) AtPT4: a fourth member of the Arabidopsis phosphate transporter gene family (accession no. U97546). (PGR 97–082). Plant Physiol 114:747

    Article  Google Scholar 

  24. 24.

    Nye PH, Tinker PB (1977) Solute movement in the soil-root system. Published by Blackwell Scientific Publications, Oxford

    Google Scholar 

Download references

Open Access

This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. L. Dotaniya.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and Permissions

About this article

Cite this article

Dotaniya, M.L., Datta, S.C., Biswas, D.R. et al. Effect of Solution Phosphorus Concentration on the Exudation of Oxalate Ions by Wheat (Triticum aestivum L.). Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 83, 305–309 (2013). https://doi.org/10.1007/s40011-012-0153-7

Download citation

Keywords

  • Citrate
  • Oxalate
  • Phosphorus
  • Wheat