Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 52, No. 359, pp. 1277-1282, June 1, 2001
© 2001 Oxford University Press

Original Papers

Plant growth and cation composition of two cultivars of spring wheat (Triticum aestivum L.) differing in P uptake efficiency

Y.-G. Zhu^1,2,3,5, S.E. Smith^1,2,3 and F.A. Smith^2,4

¹ Cooperative Research Centre for Molecular Plant Breeding, The University of Adelaide, Glen Osmond SA 5064, Australia
² Centre for Plant Root Symbioses, The University of Adelaide, Glen Osmond SA 5064, Australia
³ Department of Soil and Water, The University of Adelaide, Glen Osmond SA 5064, Australia
⁴ Department of Environmental Biology, The University of Adelaide, Glen Osmond SA 5005, Australia

Received 11 September 2000; Accepted 17 January 2001

	Abstract

Top Abstract Introduction Materials and methods Results Discussion References

 
Phosphorus (P)–zinc (Zn) interactions were investigated in two wheat cultivars (Brookton versus Krichauff) differing in P uptake efficiency. The experiment was done in a growth chamber. Rock phosphate (RP) or CaHPO₄ (CaP) were used as P sources, and ammonium nitrate (AN) or nitrate only (NO) were used as nitrogen sources. Two Zn levels were used, 0.22 mg kg^-1 (LZ) and 2.2 mg ZnSO₄.7H₂O kg^-1 (HZ), respectively. P availability significantly affected plant biomass production, but Zn supply had little effect. Plants fed ammonium nitrate had significantly lower concentrations of cations than those fed nitrate only. Cultivar Brookton (with higher P uptake efficiency) consistently had lower concentrations of cations than cv. Krichauff (with low P uptake efficiency) under limited P supply. The differences in concentrations of cations increased with the decrease in P availability, but were not affected by Zn supply. The ratio of potassium in roots to shoots of cultivar Brookton was always higher than in cultivar Krichauff. Based on these findings, it is postulated that the lower concentrations of cations in cultivar Brookton are related to root exudation of organic anions, and a conceptual model is established to describe the regulation of root exudation of organic anions and concentrations of cations.

Key words: Cation–anion balance, cation composition, phosphorus efficiency, zinc-phosphorus interaction, wheat.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
Large applications of phosphorus (P) fertilizers are the traditional way to increase crop production in low P soils. However, the utilization efficiency of P fertilizers is often very low, ranging from 10–30% in the year applied (Bolland and Gilkes, 1998), resulting in the continuous accumulation of P in soil. High soil P may pose a risk of P transport from soil to water bodies, causing toxic algal blooms (Heckrath et al., 1995; Sharpley and Rekolainen, 1997). Selecting crop cultivars with high P uptake efficiency is an alternative approach to the management of soils with low available P and to the efficient use of P fertilizers (Graham, 1984; Caradus, 1995; Lynch, 1998). There is an array of plant traits contributing to high P uptake efficiencies, among which are acidification in the rhizosphere (i.e. excretion of protons from roots) and exudation of organic anions by roots (Randall, 1995).

Cation–anion balance within the plant is an important factor regulating intracellular and/or rhizosphere pH and synthesis of organic anions (Raven and Smith, 1976; Cakmak and Marschner, 1990; Tolra et al., 1996; Graff et al., 1999). The difference between cations and anions (C–A) has been used as a parameter to quantify the organic acid content of plants (Marschner, 1995). The amounts and forms of nitrogen supply play critical roles in ionic balance within the plant (van Beusichem et al., 1988; Wollenweber and Raven, 1993; Graff et al., 1999). Other nutrients, such as Zn²⁺, Cl^– and will also affect the ionic balance (Cakmak and Marschner, 1990; Soltanpour et al., 1999). Since P uptake efficiency is related to root exudation of organic anions and excretion of protons, it is possible that plant cultivars with different P uptake efficiency would also have different compositions of cations and different cation–anion balance.

The aim of the present study was to investigate the composition of cations in two wheat cultivars with different P uptake efficiencies, and the effects of P availability, Zn supply and nitrogen sources on the composition of cations.

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Preparation of the growth medium
Laffer sand was used in this experiment because it is low in most nutrients and hence nutrient levels can be manipulated. The sand was first passed through a 0.5 mm sieve, and was then washed at least five times using Reverse Osmosis purified water (hereafter RO water). The sand was supplemented with two sets of nutrients kg^-1 sand with different nitrogen sources. (1) Nitrate only (NO): 0.918 g Ca(NO₃)₂.4H₂O, 0.174 g K₂SO₄, 0.185 g MgSO₄, 0.4 mg FeEDTA, 2 mg CuSO₄.5H₂O, 0.6 mg MnSO₄.4H₂O, 0.4 mg CoSO₄.7H₂O, 0.5 mg H₃BO₃, and H₂MoO₄.H₂O; (2) ammonium nitrate (AN): 0.918 g Ca(NO₃)₂.4H₂O was replaced by 0.444 g CaCl₂.2H₂O and 0.3 g NH₄NO₃; other nutrients remained the same. Two zinc levels were used, 0.22 and 2.2 mg ZnSO₄.7H₂O kg^-1 sand for low and high Zn supplies, respectively. Powder of CaCO₃ (0.3%) was mixed with the Laffer sand, and the final pH of the sand was around 6.8. Two P sources were compared, high P supply with 0.5 g CaHPO₄ kg^-1 sand (CaP) and low P supply with 1 g rock phosphate kg^-1 sand (RP) (particle size <250 µm, North Carolina, P content around 17%) (Table 1). Each treatment had three replicates.

View this table: [in this window] [in a new window]   Table 1. Experimental treatments used in this study

 

Growth conditions
Two cultivars of spring wheat (Triticum aestivum L.) were used, namely Brookton and Krichauff. Brookton has previously been identified as having a higher P uptake efficiency than Krichauff under the same conditions of this study (YG Zhu et al., unpublished results). Four germinated seeds were sown in each pot (6.2 cm in diameter and 26 cm in depth) filled with 1 kg of sand. Each pot was thinned to two plants 3–4 d after emergence. The experiment was conducted in a growth cabinet set at 20/15 °C day/night with 14 h of light period (260 µE m^-2 s^-1). The plants were harvested 4 weeks after emergence.

Plant analysis
After harvest, roots were thoroughly washed to remove sand particles, and plants were divided into shoots and roots. Root and shoot samples were oven-dried at 70 °C for 24 h and dry weights recorded. Tissue samples were then ground. Subsamples were digested with nitric acid (70%) and analysed by Inductively Coupled Plasma Atomic Emission (ICP-AES) for P, S, Zn, Ca, Mg, Na, and K.

Data analysis
In order to compare the balance of inorganic cations and anions, concentrations were calculated on the basis of meq kg^-1 dry mass. All data were subjected to analysis of variance (ANOVA) using PC window-based Genstat (Genstat 5 Committee, 1994).

	Results

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Plant growth
In treatments NO–RP and AN–RP, Brookton had higher shoot and root biomass than Krichauff (Table 2). Zn supply did not significantly affect biomass production, except in the treatment AN–RP, where low Zn supply reduced root biomass of both Brookton and Krichauff significantly. In the treatment NO–CaP, there were no significant differences in shoot and root biomass between the cultivars, except that with high Zn supply Krichauff had higher root biomass than Brookton. The two cultivars had similar root/shoot ratios, and Zn supply did not change the root/shoot ratios. Root/shoot ratios in treatment NO–RP were generally higher than those in treatments AN–RP and NO–CaP, irrespective of Zn supply.

View this table: [in this window] [in a new window]   Table 2. Biomass production of two wheat cultivars grown in sand culture

 

Cation composition
Brookton consistently had lower total concentrations (meq kg^-1) of major cations (Ca, Mg, Na, and K) in shoots than Krichauff in all treatments (Table 3). Furthermore, the differences between the two cultivars were much greater in RP than in CaP treatments. Concentrations of Na were very low in all treatments. In treatments RP, concentrations of Ca, Mg and K in Brookton were lower than those in Krichauff. In treatments NO–CaP, concentrations of Ca and Mg in Brookton were lower than in Krichauff, but the two cultivars had no significant differences in concentrations of K. Zn supply did not significantly affect the cation concentrations, except that concentrations of K in treatments AN–RP and NO–CaP decreased significantly in high Zn supply. With treatments RP, plants grown with ammonium nitrate (AN) always had much lower concentrations of K than those grown with nitrate only (NO) resulting in a large reduction in concentrations of total cations. Cation concentrations in cultivar Brookton grown in NO–CaP were higher than in AN–RP, mainly due to differences in K concentrations. However, this was not the case with cultivar Krichauff.

View this table: [in this window] [in a new window]   Table 3. Cation composition in shoots of two wheat cultivars grown in sand culture

 
In roots there were no significant differences in total concentrations of major cations between the two wheat cultivars (Table 4). Zn supply did not affect the concentrations of cations either in total or individually, except that in treatment AN–RP low Zn supply reduced the concentrations of Mg and K, leading to a reduction in concentrations of total cations. In RP treatments plants grown with ammonium nitrate (AN) always had much lower concentrations of K than those grown with nitrate only (NO), resulting in a very large reduction in concentrations of total cations. Cation concentration in NO–CaP treatments were much higher than in AN–RP, due to high Ca and/or K.

View this table: [in this window] [in a new window]   Table 4. Cation composition in roots of two wheat cultivars grown in sand culture

 
In treatments NO–RP and AN–RP, total concentrations of cations in Brookton were consistently lower than those in Krichauff when expressed on the whole plant basis (Table 5). In treatment NO–CaP the cultivars had similar total concentrations of cations. Zn supply did not have a significant effect on concentrations of cations within the whole plant except that in treatment AN–RP the concentrations of Mg were higher in high Zn supply than that in low Zn supply, causing a slight increase in the total concentrations of cations. In treatments with NO, plants always had higher concentrations of cations irrespective of genotypes and Zn supply.

View this table: [in this window] [in a new window]   Table 5. Cation composition within whole plants of two wheat cultivars grown in sand culture

 

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
Both cultivars grew well in NO–CaP treatments, with high P supply. In AN treatments, Brookton grew better than Krichauff. In NO–RP treatments, growth of both cultivars was greatly reduced but Brookton grew better than Krichauff. There was no effect of varying Zn. Brookton has been identified as having higher P uptake efficiency than Krichauff, based on a sand culture system using rock phosphate and CaHPO₄ (Zhu et al., 2001a, b). The results reported here demonstrate that these two cultivars had significant differences in concentrations of major cations (Ca, Mg, Na, and K) (Tables 3, 4, 5), apparently associated with the availability of P in the growth medium. With low P availability in treatments NO–RP and AN–RP, there were significant differences in the concentrations of cations between the two cultivars, and the differences in treatment NO–RP (lowest P availability) were greater than in treatment AN–RP (medium P availability). In treatment NO–CaP, in which P supply is non-limiting, differences in total concentrations of cations between cultivars were much smaller.

It is suggested that the lower concentrations of cations in Brookton can be related to its high P uptake efficiency and that previous findings that roots of Brookton can extrude more H⁺ to the rhizosphere than Krichauff (YG Zhu et al., unpublished results) is very relevant. The background to their reasoning is as follows. Three sets of net ion fluxes are involved in plant growth: (1) uptake of inorganic cations, (2) uptake of inorganic anions, and (3) extrusion or (sometimes) uptake of H⁺. Internal charge balance involves the accumulation of inorganic and organic (carboxylate) anions. Uptake of inorganic cations, especially K⁺, can be high in treatments with where charge balance during N assimilation results in accumulation of large amounts of carboxylate anions, such as citrate or malate. The alternative ‘strategy’ for uptake by plants involves net influx of H⁺, equivalent to OH^– release, and relatively low concentrations of carboxylate anions and inorganic cations such as K⁺. When NH₄⁺ is taken up, N assimilation results in large-scale production and extrusion of H⁺ and in relatively low concentrations of carboxylate anions and inorganic cations (Kirkby, 1969; Raven and Smith, 1976). In addition to these processes that are directly associated with N assimilation, there can be accumulation of carboxylate anions associated with ‘excess cation influx’, i.e. exchange of cations such as K⁺ for H⁺. All these processes collectively result in electric charge-balance internally and form a combined biophysical (membrane transport) and biochemical pH-stat (Smith and Raven, 1979). Superimposed on them, there can also be extrusion of organic acid, i.e. carboxylate anions plus H⁺, as found under conditions of nutrient stress (Marschner, 1995)

A complete balance-sheet of cation–anion uptake or balance internally cannot be provided and so it is not possible to account definitively for differences between the two cultivars with respect to cation concentrations, but it is possible to draw the following conclusions. Firstly, with respect to inorganic anions, differences in concentrations of H₂ and are only about 20 meq kg^-1 and consistent between treatments (Table 6). Uptake of Cl^– would be very small under the conditions of the experiment (see also Kirkby, 1969; Watanabe et al., 1971; van Beusichem et al., 1988). It would be expected that under the conditions of the experiment would have been almost completely reduced. Thus, it is not believed that the large differences between the cultivars in total cation concentrations in NO–RP treatments relate to differences in internal inorganic anions. Secondly, the fact that biomass production and total concentrations of cations were similar in the two cultivars when P supply was high (NO–CaP) suggests that there was nothing fundamentally different between their strategies for acquiring and assimilating under these conditions. Thirdly, the biomass production in AN–RP treatments suggests that H⁺ extrusion associated with NH₄⁺ uptake increased P availability to both cultivars. Fourthly, the higher biomass and the lower concentrations of cations in Brookton compared with Krichauff in AN treatments also suggests that the greater growth of Brookton was due to higher H⁺ extrusion, compared with Krichauff. It is logical, therefore, to conclude that the higher biomass of Brookton in NO–RP treatments is also associated with the higher H⁺ extrusion, previously demonstrated (YG Zhu et al., unpublished results). It is suggested that, in the NO–RP treatment, at least, this H⁺ is accompanied by the extrusion of carboxylate anions such as citrate or malate to the rhizosphere. In simple terms, it is believed that in the RP treatments Brookton extruded part of its carboxylates whereas Krichauff accumulated them, along with inorganic cations. This extrusion of organic anions can mobilize Ca-bound P (in this instance, rock phosphate, RP), and increase plant P uptake. This explanation is in accordance with the fact that Brookton had high P uptake efficiency when it was supplied with RP, irrespective of nitrogen supply.

View this table: [in this window] [in a new window]   Table 6. Concentrations of anions (H2+) within whole plant of two wheat cultivars grown in sand culture (meq kg-1DW)

 
This extrusion will probably involve the translocation of organic anions from shoots to roots via phloem. Phloem transport of K⁺ to roots is known to be very high (Hocking, 1980; Jeschke and Pate, 1991), and is essential for photosynthate export in the phloem (Marschner et al., 1996). Enhanced extrusion of organic anions may leave behind a relatively higher proportion of K⁺ in the root, and control the subsequent K⁺ uptake via a negative feedback (Siddiqi and Glass, 1986), resulting in lower concentrations of K⁺ in shoots. In fact this study's results indicated that K⁺ was the major contributor (over 50%) to the differences in concentrations of cations (Table 5), and that the differences in concentrations of cations between the two cultivars were significant in shoots, but not in roots (Tables 3, 4). Furthermore, the distribution of K⁺ in roots and shoots was significantly higher in Brookton than in Krichauff in treatments NO–RP and AN–RP, but not in treatment NO–CaP (Fig. 1).

View larger version (28K): [in this window] [in a new window]   Fig. 1. The distribution of K in roots and shoots of plants of two wheat cultivars grown in sand culture with different P availability. Columns with different letters are significantly different (p<0.05) according to an ANOVA test (abbreviation are the same as in Table 1).

 
Based on the above discussion, the authors postulate the conceptual model shown in Fig. 2, which illustrates the regulation of ionic balance in wheat cultivars in relation to root exudation of organic anions (and therefore to P uptake efficiency). Detailed studies are under way to examine the root exudates at different levels of phosphorus supply in Brookton and Krichauff.

View larger version (21K): [in this window] [in a new window]   Fig. 2. A schematic diagram showing the possible link between ionic balance and root exudation of protons and organic anions. A–, inorganic anions, C+ inorganic cations, RCOO–, organic anions.

 

	Acknowledgments

 
We wish to thank the Cooperative Research Centre for Molecular Plant Breeding for financial support. Technical assistance from Andrew Barritt is greatly appreciated. We also would like to thank Ms Teresa Fowles for ICP analyses.

	Notes

 
⁵ To whom correspondence should be addressed. Fax: +61 8 83036511. E-mail: yongguan.zhu{at}adelaide.edu.au

	References

Top Abstract Introduction Materials and methods Results Discussion References

 
Bolland MD, Gilkes RJ. 1998. The chemistry and agronomical effectiveness of phosphate fertilizers. Journal of Crop Production 1, 139–163.

Caradus JR. 1995. Genetic control of phosphorus uptake and phosphorus status in plants. In: Johansen C, Lee KK, Sharma KK, Subbarao GV, Kueneman EA, eds. Genetic manipulation of crop plants to enhance integrated nutrient management in cropping systems. 1. Phosphorus. Patancheru, India: ICRISAT Asia Centre, 55–74.

Cakmak I, Marschner H. 1990. Decrease in nitrate uptake and increase in proton release in zinc-deficient cotton, sunflower and buckwheat plants. Plant and Soil 129, 261–268.

Genstat 5 Committee 1994. Genstat 5 reference manual. Oxford, UK: Clarendon Press.

Graff JE, Hermann RK, Zaerr JB. 1999. Ionic balance and organic acids in western red cedar, western hemlock, and Douglas-fir seedlings grown in low- and high-N soils. Canadian Journal of Forest Research 29, 669–678.

Graham RD. 1984. Breeding for nutritional characteristics in cereals. Advances in Plant Nutrition 1, 57–102.

Heckrath G, Brooks PC, Poulton PR, Goulding KWT. 1995. Phosphorus leaching from soil containing different P concentration in Broadbalk experiment. Journal of Environmental Quality 24, 904–910.[Abstract/Free Full Text]

Hocking PJ. 1980. The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Groh). Annals of Botany 45, 633–643.[Abstract/Free Full Text]

Kirkby EA. 1969. Ion uptake and ionic balance in plants in relation to the form of nitrogen nutrition. In: Rorison I, ed. Ecological aspects of the mineral nutrition of plants. Oxford, UK: Blackwell Scientific Publications. 215–235.

Jeschke WD, Pate JS. 1991. Cation and chloride partitioning through xylem and phloem within the whole plant of Ricinus communis L. under conditions of salt stress. Journal of Experimental Botany 42, 1105–1116.[Abstract/Free Full Text]

Lynch J. 1998. The role of nutrient-efficient crops in modern agriculture. Journal of Crop Production 1, 241–264.

Marschner H. 1995. Plant nutrition of higher plants. London, UK: Academic Press.

Marschner H, Kirkby EA, Cakmak I. 1996. Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. Journal of Experimental Botany 47, 1255–1263.

Randall PJ. 1995. Genotypic differences in phosphate uptake. In: Johansen C, Lee KK, Sharma KK, Subbarao GV, Kueneman EA, eds. Genetic manipulation of crop plants to enhance integrated nutrient management in cropping systems. 1. Phosphorus. Patancheru, India: ICRISAT Asia Centre, 31–48.

Raven JA, Smith FA. 1976. Nitrogen assimilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytologist 76, 415–431.[Web of Science]

Sharpley AN, Rekolainen S. 1997. Phosphorus in agriculture and its environmental implications. In: Tunney H, Carton OT, Brooks PC, Johnston AE, eds. Phosphorus loss from soil to water. UK: CAB International, 1–47.

Siddiqi MY, Glass ADM. 1986. A model for the regulation of K⁺ influx and tissue potassium concentrations by negative feedback effects upon plasmalemma influx. Plant Physiology 81, 1–7.[Abstract/Free Full Text]

Smith FA, Raven JA. 1979. Intracellular pH and its regulation. Annual Review of Plant Physiology 30, 289–311.[Web of Science]

Soltanpour PN, Al-Wardy MM, Ippolito JA, Rodriguez JB, Self J, Gillaume M, Mathews D. 1999. Chloride versus sulfate salinity effects on alfalfa shoot growth and ionic balance. Soil Science Society of America Journal 63, 111–116.[Abstract/Free Full Text]

Tolra RP, Poschenrieder C, Barcelo J. 1996. Zinc hyperaccumulation in Thlaspi caerulescens. II. Influence on organic acids. Journal of Plant Nutrition 19, 1541–1550.

Van Beusichem ML, Kirkby EA, Baas R. 1988. Influence of nitrate and ammonium nutrition on the uptake, assimilation, and distribution of nutrients in Ricinus communis. Plant Physiology 86, 914–921.[Abstract/Free Full Text]

Watanabe FS, Olsen SR, Cole CV. 1971. Ionic balance and growth of five plant species in four soils. Agronomy Journal 63, 23–28.[Abstract/Free Full Text]

Wollenweber B, Raven JA. 1993. Implications of N acquisition from atmospheric NH₃ for acid-base and cation–anion balance of Lolium perenne. Physiologia Plantarum 89, 519–523.

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