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Progress in selected areas of rhizosphere research on P acquisition.

Introduction

Essentially all soils require regular inputs of fertiliser or manure P to raise their solution P concentration such that P can be transported to plant roots at rates sufficient to meet requirements for continuous crop production.

The efficiency of fertiliser P utilisation by crop plants is low compared with the utilisation of fertiliser nitrogen. Most crop trials show that only 5-30% of the soluble P applied to soils is recovered in the first crop, leaving 70-95% of the P applied as 'fertiliser-soil reaction products' in the soil for the next growing season (Cooke 1970; Bolland and Gilkes 1998). Long-term fertiliser trials demonstrate that the plant availability of this fertiliser--soil reaction product P in the following season is considerably lower (by 20-70%) than that of freshly applied soluble P and continues to decline over a number of years (Rajan et al. 1991; Bolland and Gilkes 1998). For example, in New Zealand hill country pastures, to support sheep and beef production at 10-12 stock units per hectare, approximately 15-20 kg P/ha.year is required to maintain the plant-available soil P status (as indicated by Olsen P soil test values). Annual product losses of P leaving the farm as meat and wool are 2-4 kg P/ha.year. The remaining P accumulates in the soil as inorganic and organic P compounds at the rate of 12-15 kg P/ha.year (Moir et al. 1997). It is common in fields that have received fertiliser for 50-60 years that the total P content of these pastoral topsoils has increased by 600-1000 mg P/kg (Moir et al. 1997).

It remains unclear to what extent the different forms of P (P adsorbed by hydrous oxides of Fe and Al on soil particle surfaces, P associated with more discrete Ca-based soil fertiliser reaction products, and/or these forms additionally complexed with soil organic matter) in this large accumulated reserve contribute to sustaining the plant-available pool.

This large reserve of soil P that has accumulated in soils developed for agricultural use appears to be an inefficient use of fertiliser P, particularly as the current use of P fertiliser world-wide (16 Tg/year) is projected (Baanante and Hellums 1998) to have to increase by more than 1.43-fold by 2025 to meet the food requirement of the expanding global population (another 2.4 billion mouths).

The decrease in commercially mineable resources of high-grade phosphate rocks (PR) will increase the future cost of manufactured soluble P fertiliser as lower grade, less easily beneficiated sources are mined for agricultural use (Cook 1998). To exacerbate the problem, it is the small-scale farmers in developing countries of the tropics and subtropics farming high P-requiring, P-deficient Oxisols and Ultisols that are expected to meet the bulk of the increased demand in food production (FAO 1987; Stangel and von Uexkull 1990; Runge-Metzger 1995). In addition, these impoverished land users often cannot afford to pay for expensive manufactured fertilisers and would benefit from agricultural technology that allows use of the low cost, lower quality PRs for direct application on suitable acid soils.

Thus, there has been, and still is, ample justification for research directed at identifying plant species and plant mechanisms that improve the ability of plants to utilise sparingly soluble forms of soil and fertiliser P. The chemical properties of solid-phase soil P are diverse, including inorganic P strongly adsorbed or chemisorbed on amorphous hydrous oxides of Fe and Al, discrete more crystalline phases of P (which tend to be dominantly Fe and Al phosphates in more strongly weathered acid soils but include more Ca phosphates in less weathered weakly acidic and neutral to alkaline soils), and complex mixtures of organic P. The organic P can also be present in an adsorbed form--some is present as discrete low-molecular-weight ions adsorbed on the hydrous oxide surfaces; however, the majority of organic P is present as humic and fulvic organo-metallic P complexes (see reviews by Hedley et al. 1995; Frossard et al. 1995, 2000; Hinsinger 2001). This diverse nature of P forms indicates that several different solubilising strategies can be used by plant roots and their associated microflora. Research is required to identify plants that employ successful soil P solubilisation strategies. Knowledge of such mechanisms may allow the external P uptake efficiency (a greater ability to recover P from the soil) of agriculturally important plants to be improved.

The accumulating, sparingly soluble soil P cannot move to roots, therefore roots must grow to and solubilise this P. Mechanisms that will enhance this (adapted from Hedley et al. 1994) are the ability of the plant root system to:

(1) develop long, fine, hairy roots;

(2) multiply roots in soil zones containing plant-available P;

(3) be able to solubilise inorganic P (Pi) through changes in pH or through the release of chelating agents;

(4) utilise soil organic P (Po) through the release of hydrolytic enzymes; and

(5) associate with mycorrhizal fungi.

In this paper we review our research and that of others on rhizosphere processes capable of transforming the accumulating soil P reserve and low cost PR into P effective for plant growth. For readers whose research interests lie in this area we recommend also reading a recent review by Hinsinger (2001).

P-efficient root structures

A general response to P deficiency is increased root: shoot ratios; however, selection in favour of this would be likely to reduce above-ground yield. A better strategy would be to select for a greater absorbing surface per unit mass of roots. Simple mathematics dictate that, for a given root mass, long fine roots provide a greater absorbing surface than short coarse ones, as shown in equation below (from Kirk et al. 1998). Let r, l, and [rho] be root radius, length, and density, respectively:

Surface area = 2[pi]rl and mass (m) = [rho][pi][r.sup.2]l

Therefore, surface area = 2m/([rho]r)

Therefore, one plant breeding strategy would be to breed plants with long, fine, hairy roots. Plants can increase the length and fineness of their roots (Garcia and Ascencio 1992; Ciereszko et al. 2002) or the length and density of their root hairs (Foehse and Jungk 1983) in response to P deficiency and it seems probable that cultivar differences could be exploited (Kirk et al. 1998). Wissuwa and Ae (2001) identified a P-efficient line of rice (Oryza sativa) that took up 3-4 times more P from a P-deficient volcanic soil than the cultivar Nipponbare. When grown on the P-deficient soil, the P-efficient line had a root surface area approximately 50% of that of the non-P-stressed treatment, whereas the root surface area of the cultivar Nipponbare declined by >80%. The poorer growth of Nipponbare was probably the result of insufficient P uptake to sustain plant growth, including root growth. Wissuwa and Ae (2001) concluded that the genotypic differences in the ability of rice to maintain root growth were therefore likely caused by some mechanism that increased the efficiency of roots to access forms of P not readily available.

The presence of root hairs further increases the amount of absorbing surface. Gahoonia and Nielsen (1997) studied 2 barley (Hordeum vulgare) cultivars that differed widely in their ability to extract P from low P soil in field conditions. Plants of the cultivar Salka depleted twice as much P from the rhizosphere as did plants of the cultivar Zita, which was attributed to Salka plants having longer root hairs (1.10 v. 0.63 mm) at a greater density (32 v. 21 root hairs/mm root) than Zita plants. Similarly, Gahoonia et al. (1997) obtained significant (P < 0.01) correlations between root hair length and the amount of rhizosphere P depleted when comparing among 3 wheat cultivars and 3 barley cultivars. This correlation was particularly strong in soil with a low P status ([R.sup.2] = 0.99 for wheat and 0.95 for barley). Recent research by Bates and Lynch (2000) and Ma et al. (2001) has shown that Arabidopsis thaliana roots developed longer and denser root hairs in response to low P status. The mechanism involved an increase in both the number of trichoblasts (undifferentiated cells with the potential to form hairs) and the percentage of trichoblasts that formed root hairs in the low P environment.

Plants are also able to concentrate their roots in P-fertilised zones (Anghinoni and Barber 1980), presumably by chemotropism. This response enables them to take up more P than if their roots were randomly or equally distributed throughout the soil. Ge et al. (2000), however, discussed how root architecture is principally controlled by gravitropism, where gravitropism determines the depth at which laterals form. In some genotypes of common bean (Phaseolus vulgaris) P deficiency can reduce root sensitivity to gravitropism (Bonser et al. 1996). Such a response can improve the external P efficiency of the root system because the resulting shallower root systems explore the higher P concentration of the upper soil layers. In addition, Ge et al. (2000) modelled the gravitropic effect on root system development and demonstrated that there would be less overlap of P depletion zones around lateral roots in shallower root systems. Shallower, fine root systems would, therefore, appear to be the most efficient in soil P acquisition, provided the water relations of the shallow soil layer did not drop below wilting point.

Thus, it would appear that gravitropic responses and chemotropic responses to low and high P status soil influence the architecture of the root system and root hair development. According to Lynch and Brown (2001), research exploring the genetic control of plant sensitivity to these responses has resulted in cultivars that produce root systems with very efficient P uptake. These cultivars are now being trialled in low P status soils in Africa and Latin America.

Factors affecting root length

The ability of plant species to express their genetic potential to produce nutrient-efficient root structures is modified by the soil physical, chemical, and biological properties. Much of our research has focussed on the effect of soil chemical properties, specifically acidic soils with low a P status, on the efficiency of P uptake by roots. Therefore, the following discussion concentrates on the soil chemical interactions with root growth, with just a brief mention of soil physical properties. The effect of biological properties, specifically mycorrhizae, on increasing effective 'root' length is discussed towards the end of the paper.

Physical

Soil physical factors that reduce root length have been discussed by Passioura (2002). These factors include excessively firm or loose soil, excessively large pores, low soil oxygen concentrations, and low soil moisture. A study by Arvidsson (1999) showed that P uptake was reduced in both excessively firm and excessively loose soil. Recognising these effects, recent models of root distribution in soils to predict nutrient uptake are accounting for physical factors [e.g. the model of Albrecht et al. (2002) for Zn and Mn uptake].

Chemical

In acidic soils, particularly at pH below 4.8, monomeric A1 concentrations in soil solution increase exponentially as pH decreases (Fig. 1a), and can reduce root growth (see reviews by Kinraide 1997; de la Fuente-Martinez and Herrera-Estrella 1999; Rout et al. 2001; Barcelo and Poschenrieder 2002). Al[O.sub.4][Al.sub.12][(OH).sub.24][([H.sub.2]O).sub.12.sup.7+] has been shown to be highly toxic in solution culture, but in soils the main phytotoxic species is [Al.sup.3+]. Recent research (Kinraide 1997) suggests that Al[(OH).sup.2+] and Al[(OH).sub.2.sup.+] are not toxic at achievable activities, but that the apparent toxicity of these species suggested in some experiments is a consequence of the relief of H+ toxicity by [Al.sup.3+] (and vice versa). The symptoms of Al toxicity on plants are swollen, stunted, and crooked roots, and a lack of feeder roots (von Uexkull 1986) and root hairs (Brady et al. 1992); thus, the ability of a plant to take up P, as well as water and other nutrients, is impaired. In the plant, free Al binds strongly to P groups in nucleic acids inhibiting division of the germ cells at the root tip (Morimura et al. 1978), affects phosphokinase and ATPase activity (Mengel and Kirkby 1982), and inhibits uptake of Ca and damages the plasma membrane of younger and outer cells in roots (Wagatsuma et al. 1995).

Plant Al tolerance varies with: plant species (Foy 1971; Gill et al. 1991; Rao et al. 1993), genotype (Mackay et al. 1990; Sivaguru and Paliwal 1993), and age (Coronel et al. 1990). Many plants that are tolerant of high soil Al concentrations (e.g. upland rice; Rao et al. 1993) are also efficient at extracting P from acidic, low P soils (Ae et al. 1995). For example, our studies (Wang et al. 1999) have shown that lucerne (Medicago sativa) root extension is inhibited by low concentrations (50-60 [micro]M) of monomeric Al found in the soil solution of New Zealand hill soils with pH in the range 5-4.8 (Fig. la, b). Manoharan et al. (1996) found that barley roots were more tolerant; however, upland rice root extension will continue even when monomeric Al concentrations reach 1500 [micro]M in soil solution (Trolove 2000) (Fig. 1b).

In many cases, growth of Al-tolerant roots is associated with the release of organic anions or phenolic compounds from the roots (Miyasaka et al. 1991; Koyama et al. 2000; Barcelo and Poschenrieder 2002). Organic anion release can also increase the availability of soil P (see later discussion); however, the location of organic anion release differs between the 2 mechanisms (Barcelo and Poschenrieder 2002)--for Al-tolerance the organic anions are released from the root tip, and for P deficiency the organic anions are normally released from the root hair zone or from proteoid roots. Much of the increase in P availability may be associated with Al-tolerant plants growing longer roots and root hairs than Al-intolerant plants in soils with high soil solution concentrations of monomeric Al.

The response of roots to monomeric Al concentration can be modified by soil solution Ca concentration. Calcium deficiency inhibits root growth (Presley and Leonard 1948). Calcium is required in large quantities to build the walls of cells in the cell elongation zone behind the root cap (Takahashi et al. 1992) and since Ca is moved largely in the xylem and only to a very limited extent in the phloem (Kirkby and Pilbeam 1984) a continual supply of Ca must be maintained to the root tip. Most soils usually contain an adequate concentration of Ca for root growth; however, in strongly weathered acidic soils, the activity of the [Ca.sup.2+] ion in solution relative to the sum of the activities of [Ca.sup.2+], [Mg.sup.2+], [K.sup.+], and [Na.sup.+] ions (Bruce et al. 1988) may be insufficient for root elongation. Liming soils will detoxify monomeric Al through formation of Al hydroxy polymer precipitates and increasing Ca concentrations in soil solution. Often the rate of root extension is better explained by the monomeric Al:Ca ratio of activities in soil solution (Hutton 1985; Manoharan et al. 1996), or molar concentrations (Wang et al. 1999). Use of Ca-based waste products (Wang et al. 1999) and P fertilisers (Manoharan et al. 1996) can also decrease Al toxicity partly by precipitating Al and partly by creating the chemical environment for non-toxic species of Al to form in soil solution. Manoharan et al. (1996) noted that barley root growth was greater in soil well fertilised with P than in unfertilised soil, despite the fertilised soil having higher concentrations of Al in soil solution. The authors attributed the apparent lower toxicity of Al in the fertilised soil to greater concentrations of less-toxic AlF complexes in soil solution derived from F applied in the P fertiliser. The choices of plant species and soil acidity management are, therefore, important considerations in creating the appropriate root architecture for P acquisition from soil.

An additional factor to consider is that roots have other important functions that can be of equal importance to root absorbing surface area in relation to P uptake from soil. Plant P uptake is limited by the P concentration gradient and the diffusivity of the P ion in soil adjacent to the root (Tinker and Nye 2000). The ability of plants to raise the P ion concentration in the rhizosphere by solubilisation of soil P will accelerate P diffusion towards the low P concentration maintained at the root surface and therefore enhance P uptake.

Rhizosphere mobilisation of acid-soluble soil and fertiliser P

The ability of plants to solubilise Pi by acidifying the rhizosphere has been well documented (e.g. Aguilar and van Diest 1981; Hedley et al. 1982a, 1983; Gahoonia and Nielsen 1992). In these studies, the mason for the acidification was due to an excess cation over anion uptake (alkaline uptake pattern), which led to the release of H+ ions to maintain electroneutrality inside the plant. For many non-leguminous plants, the amount of acidification in the rhizosphere can be dictated by the ratio of N[H.sub.4.sup.+] to N[O.sub.3.sup.-] taken up by the plant (Gahoonia and Nielsen 1992). A few plants, however, have natural alkaline uptake patterns accumulating an excess of cations over anions by a high uptake of [Ca.sup.2+], [K.sup.+], or [Mg.sup.2+]. This uptake pattern probably results from the dissociation of carboxylic acid functional groups on organic compounds synthesised as part of plant growth. Functional groups that dissociate cause the plant internal acidity problems and a H+ ion is released from roots in exchange for the uptake of a mineral cation from soil solution (Haynes 1990; Bolan and Hedley 2002). This is the case with many temperate legumes in which the demand for increased cation uptake appears to be produced by the requirement to balance the negative charge on shoot-accumulated, dissociated carboxylic acid groups of strong amino acids such as aspartate and glutamate and other structural organic acids (Bolan and Hedley 2002). In other plants, such as Brassica napus, the alkaline uptake pattern can be invoked by P deficiency (Hedley et al. 1982b). For mycorrhizal plants, hyphal uptake of N[H.sub.4.sup.+] can also cause acidification of the rhizosphere (Li et al. 1991) and increased P uptake in an alkaline soil (see later discussion).

Rhizosphere acidification, however, does not always result in extra P release to plant roots. In their study on upland rice, Hedley et al. (1994) found that the amount of P uptake that was explained by rhizosphere acidification was relatively small in a strongly weathered Ultisol.

The amount of P released by acidification in the rhizosphere is dependent on both the amount of acid released, or generated in the rhizosphere, and the amount of acid-soluble P in the soil. Highly weathered soils, such as Ultisols or Oxisols, contain minimal amounts of acid soluble P. Hedley et al. (1994) used the fine mesh technique (Fig. 2) in root study containers (originally developed by Kuchenbuch and Jungk 1982) to develop a planar upland rice rhizosphere in which the depletion of soil and fertiliser P fractions could be studied. Zoysa et al. (1999) used a similar technique with tea (Camellia sinensis) seedlings. Both studies used strongly weathered Utlisols ([MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] 4.5-4.6) containing 28-37 mg P/kg soil (5-9% of their total soil P) in the acid-soluble fraction. In both studies there was negligible rhizosphere-induced depletion of the acid-soluble P pool. However, when the acid-soluble P pool was increased by PR addition (200 mg P/kg soil), approximately 25% dissolution of the PR occurred in the rhizosphere soil, which was double the rate of dissolution in non-rhizosphere soil (Zoysa et al. 1999). Using similar techniques with a New Zealand hill soil (Typic Dystocrept, [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] 5.3) Trolove et al. (1996) demonstrated that acidification of white clover (Trifolium repens) and lotus (Lotus pedunculatus) rhizospheres (Fig. 3) caused accelerated dissolution of North Carolina reactive PR (Fig. 4). In the rhizosphere of the unfertilised soil, however, dissolution of the small amount of native acid-soluble P (23 mg P/kg soil) was not significant.

In a UK soil ([MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] 6.2) that contained 151 mg P/kg soil (approx. 13% of its total P) in acid-soluble form, Hedley et al. (1982b) used the thin-layer rhizosphere technique (Fig. 5) to show that decreased pH in the rhizosphere of fodder rape (Brassica napus) provided much of the plant P requirement by causing approximately 32% dissolution of the acid-soluble soil P fraction. In vitro P desorption experiments carried out at different solution pH confirmed that rhizosphere acidification could account for the extra soil P released in the rhizosphere and taken up by fodder rape seedlings. In an Ultisol (Hedley et al. 1994), however, the P release to upland rice could not be accounted for by the small amounts of P that can be desorbed at the acidic rhizosphere pH.

Rhizosphere acidification appears to be common amongst many plant species, especially temperate legumes; however, whether it is a mechanism effective at increasing the plant's P supply depends on the presence of acid-soluble soil P. Unless PRs are used as fertiliser, moderately and strongly weathered soils of temperate and tropical climates have little acid-soluble P, with most of their P being associated with hydrous oxides of Fe and Al (Hedley et al. 1995). Inorganic P and organic P associated with amorphous hydrous oxides of Fe and Al form the major part of the soil P extracted by 0.1 M NaOH in the P fractionation procedure used in most of our studies. This fraction is the major sink for applied soluble fertiliser P (Hedley et al. 1994; Trolove et al. 1996).

Rhizosphere mobilisation of inorganic P associated with hydrous oxide surfaces

In both unfertilised and recently fertilised soils, the inorganic P component associated with hydrous oxide surfaces was depleted in rhizosphere studies with fodder rape (Hedley et al. 1982b, 1983), upland rice (Hedley et al. 1994), white clover and lotus (Trolove et al. 1996), and tea (Camellia sinensis), Camellia japonica, Calliandra calothyrsus, Guinea grass (Panicum maximum), and bean (Phaseolus vulgarus) (Zoysa et al. 1998). In studies with upland rice (Hedley et al. 1994), all soluble P entering the 0.1 M NaOH Pi fraction after fertilisation with monocalcium phosphate (MCP) was depleted in the slice of soil adjacent to the rice rhizoplane (Fig. 6). Zoysa et al. (1998) observed the same high degree of depletion of Pi that had accumulated in the NaOH-Pi fraction after PR dissolution, with tea and guinea grass causing the greatest depletion of this fraction. Both Hedley et al. (1994) and Trolove (2000) have demonstrated that, for the Philippine Ultisol used, it was impossible to simulate this level of P depletion by dilution desorption at the rhizosphere pH. However, batch extraction of the soil with citrate (Hedley et al. 1994) and dilution desorption experiments with varying citrate concentrations (Trolove 2000) (Fig. 7) clearly demonstrated that the presence of citrate was quite capable of raising the soil solution P concentration 10-fold compared with 0.01 M Ca[Cl.sub.2]. Several experiments have been undertaken to identify whether root release of organic acids could solubilise P for plants growing in these more strongly weathered soils (e.g. Bolan et al. 1994, 1997; Kirk et al. 1999a). Bolan et al. (1997) identified elevated concentrations of acetate, citrate, lactate, malate, oxalate, and formate in rhizosphere soil of 98-day-old lotus seedlings compared with soil incubated without plants for 98 days (Table 1).

Lin and You (1989) studied the composition of exudates from 4 cultivars of lowland rice and found that the major compounds released were sugars, plus organic acids and amino acids, with the 3 basic amino acids comprising a large proportion of the amino acids released (Table 2). Liu et al. (1990) found that citric acid was the dominant acid released by rice, and that the amount of citric acid released increased in the absence of P. Kirk et al. (1999b) also measured significant amounts of citrate released from upland rice roots grown in the same soil as used in the study by Hedley et al. (1994). Kirk (1999) has since developed an elegant model of root-released citrate solubilisation of soil P to explain the soil P depletion profiles measured by Hedley et al. (1994) in the upland rice rhizosphere (Fig. 8).

The action of root-released organic acids

The ability of low-molecular weight organic acids to increase the amount of P in the soil solution has been well documented (e.g. Deb and Datta 1967; Traina et al. 1986; Jones and Darrah 1994; Hinsinger 2001). Traina et al. (1986) identified 3 possible mechanisms by which organic acids increase the level of P in solution. These include:

* competition for P adsorption sites

* dissolution of adsorbents

* changes in the surface charge of the absorbents.

Organic anions, particularly citrate, may reduce the amount of P bound to the soil, and consequently increase the amount of P in solution, by competing for adsorption sites (Nagarajah et al. 1970; Parfitt 1979; Lopez Hernandez et al. 1986; He et al. 1992). For example, Bolan et al. (1994) observed that the adsorption of P by 2 New Zealand soils was decreased by the addition of simple carboxylic acids (citrate, oxalate, tartrate, malate, lactate, and formate). Adsorption of organic anions by variable-charge soils has been shown to increase the amount of negative charge on the surface (Shanmuganathan and Oades 1983), which further decreases the adsorption of the [H.sub.2]P[O.sub.4.sup.-] ion (Nagarajah et al. 1968).

Organic acids can enhance the release of P through the dissolution of Ca-phosphates and positively charged surfaces of hydrous oxides of Fe or Al (Earl et al. 1979; Fox et al. 1990; Jones and Darrah 1994), or Fe/Al-humic compounds (Gerke 1992). The effectiveness of an organic compound in complexing metal ions is dependent upon the number and position of the carboxylic and phenolic groups in the organic acid.

Associated [H.sup.+] ions may also assist in the dissolution process. Jones and Darrah (1994) for example, found that citric acid addition (undissociated citric acid) solubilised more P from a soil rich in Ca-P minerals than could be attributed to the sum of the P solubilised by the action of [H.sup.+] ions and by Na-citrate.

Relative effectiveness of various organic compounds at releasing P

In general, organic compounds containing tri-carboxylic acids are more effective at solubilising P than those containing di-carboxylic acids, which are in turn more effective than mono-carboxylic acids. For example, Bolan et al. (1994) found that citric acid, a tricarboxylic organic acid, was more effective at solubilising P from both an allophanic soil and a soil dominated by vermiculite, than dicarboxylic acids. The extent of solubilisation of P by organic acids was in the order citrate > oxalate = tartarate = malate > lactate = formate. Parfitt (1979) also found citrate to be more effective than oxalic acid (a dicarboxylic acid) in desorbing P from goethite. Under some conditions, oxalic acid has been found to be more effective than citric acid. Strom et al. (1994, 2002) found that oxalic acid extracted markedly more P from an alkaline Rendzic Leptosol ([MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] 8.0) than did other organic acids, including citric acid. Nagarajah et al. (1970) found that citric acid was more effective than other organic acids in reducing P sorbed to goethite and gibbsite, but oxalate was markedly more effective in reducing P sorbed to kaolinite.

Fox et al. (1990) measured the amount of P solubilised by a range of organic acids from a soil rich in Al-oxides. They found that the amount of P extracted by organic acids was proportional to the stability (log [K.sub.Al]) of the Al-organate reaction product. Below a log [K.sub.Al] value of 4, there was no difference in the amount of P extracted by a solution containing organic acids or distilled water. Similarly, Bolan et al. (1994) obtained an exponential decrease in the amount of P adsorbed by an Allophanic soil with an increase in the log [K.sub.Al] value of the Al-organate. This effect is attributed to the chelation of Fe and Al (Fig. 7) from the absorbing, hydrous oxide surfaces coating soil particles.

Soil pH and the charge on the organic anion also play an important part on the ability of the organic acid/anion to release P from the soil. Nagarajah et al. (1970) found that the reduction in the amount of P sorbed on kaolinite, gibbsite, or goethite due to the addition of organic acids is greatest at the pH that corresponds roughly to the second pK value of the organic acid (pH 4-6 for many organic acids). The pH also influences the amount of P desorbed because it affects the stability of the reaction products. Iron-citrate complexes are stable below pH 6.8, and Jones et al. (1996a) found that the amount of Fe[(OH).sub.3] solubilised by citrate markedly increased as the pH dropped below 6.8. At a high pH of approximately 8 and above, citrate is strongly negatively charged ([3.sup.-]); studies at this pH have found that the major mechanism by which citrate releases P is by competing with P for adsorption sites (Kafkafi et al. 1988; He et al. 1992) and by citrate-induced increases in the soil surface negative charge.

Influence of soil properties on the solubilising ability of organic acids

The soil mineralogy determines the number and types of P absorbing sites, the amount of variable charge on the soil, and the extent to which the P-sorbing mineral can be solubilised by the organic acid. For example, Earl et al. (1979) found that an application of citrate resulted in a greater desorption of P from Fe-rich soils than from Al-rich soils. Ae et al. (1990) grew a range of crops on an Alfisol, which contained mainly Fe-P, and a Vertisol, which contained both Ca-P and Fe-P. Pigeonpea grew well and took up adequate P on the Alfisol, whereas sorghum, soybean, pearl millet, and maize all had very low P contents and died within a month. On the Vertisol, pigeonpea had a lower P content than all the other crops. Pigeonpea roots were shown to exude piscidic acid, which was not present in soybean and sorghum root exudates. Piscidic acid and some derivatives were shown to release P from Fe-phosphates. The mineralogy also affects the diffusion rate of both the organic anion and the metal-organate complex through the soil. These rates determine the volume of soil around a root from which P can be solubilised.

The amount of P solubilised per mole of organic acid added (mobilisation efficiency) is also dependent on the initial P content of the soil. Soils with low P contents are more strongly buffered with respect to P, especially high P-fixing soils, and therefore the mobilisation efficiency of organic acids will be lower on low P soils compared with high P soils (Earl et al. 1979; Parfitt 1979; Kirk 1999).

The microbial population of the soil influences the longevity of organic acids in soil. Organic acids released by roots may provide energy sources for the rhizosphere microbial population and consequently be decomposed. Decomposition of citrate was a reason given for citrate being less effective than oxalate in stimulating P uptake by maize (Strom et al. 2002). Conversely, rhizosphere bacteria may be a source of organic acids. Lin and You (1989) also found that the presence of [N.sub.2]-fixing bacteria in the rhizosphere could stimulate the production of organic acids from roots. Rhizosphere bacteria (Kucey et al. 1989) and ectomycorrhizal fungi (Graustein et al. 1977) can also produce P-solubilising organic acids.

Amounts of organic acids released

The measurable amounts of organic acids in rhizosphere soils are often quite low, 1 [micro]mol/g soil or less (Tables 1 and 2). Measurable citrate concentrations in the rhizosphere of upland rice range from 0.07 to 0.6 [micro]mol citrate/g soil (Kirk et al. 1999a). Even in the proteoid root clusters of white lupin, where the total amount of citrate excreted is up to 23% of the total dry mass of the plant, the total citrate concentration only amounts to 1.1 [micro]mol citrate/g soil (Dinkelaker et al. 1989). In these clusters there is a large decrease in available P (due to solubilisation and plant uptake) and an increase in available Fe, Zn, and Mn. Experiments by Amann and Amberger (1988), however, suggested that a minimum citrate concentration of 5.3 [micro]mol/g soil was necessary to increase the concentration of P in solution. However, in both the experiments of Kirk et al. (1999b) and of Dinkelaker et al. (1989), P uptake was attributed to the release of organic anions. It appears, therefore, that the soil organic acid concentration required for P release is highly variable between soils, depending strongly on factors such as mineralogy and microbial activity relating to the synthesis and decomposition of organic anions (see later discussion). The lack of consensus on the concentration of citrate required to solubilise P in the rhizosphere may also result from the difficulties in recovering and measuring citrate concentrations in soils.

Factors affecting the amount of organic anions released

Root biomass

First and foremost, it should be mentioned that as a general rule, the amount of exudates released from roots is proportional to the root biomass (Vancura 1988).

Concentration of root exudates in the rhizosphere

Meshkov (1952, 1956, as cited by Vancura 1988) found that the amount of exudates released from maize and pea roots increased by 35-135% and 170-300%, respectively, if the nutrient solutions were renewed (see also Prikryl and Vancura 1980). Similarly, the amount of carbon (C) compounds exuded by roots increases in the presence of microorganisms (Barber and Lynch 1977; Vancura et al. 1977). These observations suggest that the rate of release of C compounds from the root may be regulated by an inverse relationship (feedback inhibition) with the concentration of C compounds in the rhizosphere.

Rhizosphere microorganisms

Rhizosphere microorganisms can have many different effects on the amount and composition of organic anions in the rhizosphere. Meharg and Killham (1995) found that rhizosphere microorganisms that did not infect roots could enhance root exudation several-fold, depending on population density and composition. O'Keefe and Sylvia (1992) and Azaizeh et al. (1995) found that the organic acid composition in the rhizosphere of roots colonised by arbuscular mycorrhizal (AM) fungi was not significantly different from uncolonised roots, whereas Marschner et al. (1997) detected fewer compounds in the rhizosphere of mycorrhizal roots, compared with non-mycorrhizal roots. Synergistic interactions also occur: Kim et al. (1998) found little difference in oxalate, citrate, or 2-keto-D-gluconate concentration in the rhizosphere of tomato plants inoculated with either a P-solubilising bacteria (Enterobacter agglomerans) or an AM (Glomus etunicatum) compared with the uninoculated control. However, when the plants were inoculated with both E. agglomerans and G. etunicatum, the amounts of the aforementioned organic acids released increased several-fold, depending on the age of the plant.

Temperature and light

Rovira (1959) and Schroth et al. (1966) found that the amount of root exudates released increased as the temperature increased. Sudden temperature changes, e.g. cold shock or heat shock, may also cause increased exudation (Vancura 1967). Light intensity and photoperiod (Vancura 1988) also affect the composition and quantity of root exudates. It is important to consider these factors when planning experiments to study the rate of root exudation. For example, the time taken for transferring plants from a glasshouse to a laboratory (change in temperature and light intensity) should be kept constant and be carried out at the same time of day prior to analysing the soil for organic acid concentration.

P stress

The rate of release of organic acids from roots increases when the plant is subjected to P stress. For example, Lipton et al. (1987) found that the rate of citrate release from alfalfa roots increased by 182% when grown in nutrient solution containing one-tenth of the original P (0.01 mm N[H.sub.4][H.sub.2]P[O.sub.4]) solution. However, Kirk et al. (1999a) found no consistent effect (across a range of cultivars) of the presence or absence of P on the amount of citric acid released by rice grown in solution culture.

Temporal? water stress

The amount of root exudates increases when plants are temporarily exposed to water stress (Vancura 1988). Martin (1977a, 1977b) found that zones lacking in water contained larger amounts of C exuded in the form of mucigel and in a form originating from the lysis of root tissues, compared with zones that had been well supplied with water. Presumably this mucigel is exuded to maintain root-soil contact as the water-stressed root cells lose turgor.

High [Al.sup.3+] concentrations High solution concentrations of Al have also been shown to increase the release of citric acid from Al-tolerant snapbeans (Miyasaka et al. 1991, see earlier discussion on factors affecting root length).

Mechanism of organic acid/anion release

Under most growing conditions it appears that organic anions are excreted via membrane-bound 'permease' proteins. This is discussed in detail in the review by Ryan et al. (2001). Some organic anions may be exuded by exocytosis (the process where a vesicle fuses with the plasma membrane and releases its contents outside the cell), but little is known about this process. Simple diffusion of organic anions across the plasma membrane cannot explain the quantities of organic anions exuded by plant roots because cell membranes are virtually impermeable to ions.

In highly P-stressed plants, Ratnayake et al. (1978) and Graham et al. (1981) demonstrated that the root membranes became more leaky [shown by increased [sup.86]Rb efflux (a tracer for K) and a decrease in phospholipid P content], which led to increased exudation of reducing sugars and amino acids. No organic acid analyses were performed to determine whether the membranes had become 'selectively leaky', i.e. there was no comparison between the composition of the reducing sugars and amino acids released with that of the cytoplasm. Kirk et al. (1999a) showed that the composition of exudates from both P-stressed and non-P-stressed rice roots is different from root cell composition, which suggests active exudation, or 'selective leaking' rather than simple leakage of the cellular contents through the cell membrane. In most 'normal' growing conditions, it is likely that large quantities of organic acids are released by active exudation. Gallmetzer et al. (1998), studying the efflux of citrate from Penicillium simplicissimum, a citrate-producing fungus, found that hyphae grown in solutions treated with the metabolism inhibitors N-ethylmaleimide or sodium azide had a much higher intracellular citrate concentration than the untreated control, yet markedly lower citrate excretion rates. These findings led to the hypothesis that citrate exudation is not due to an unspecific change in the permeability of the plasma membrane, nor to simple diffusion of undissociated citric acid, but is mediated by an energy-requiring transport protein.

Form released.' anion or acid?

Inside the root cell, organic 'acids' would exist as anions, since the pK values of most organic acids are 3.0-4.5, which is well below the cytoplasmic pH of 6.5-7.5 (Smith and Raven 1979). When these organic anions are exuded, they must be balanced by the release of cations from roots to maintain electroneutrality inside the cell. In many experiments, the pH of the rhizosphere declines with organic acid release, suggesting that H+ is the balancing cation. However, under Al toxicity no decrease in rhizosphere pH is observed with organic anion release, and it appears that K* is the balancing cation released from roots (Jones 1998).

In the soil, most organic 'acids' will therefore be present as organic anions, since the pH of most soils is above 4.5. However, in much of the literature, the term 'organic acid' is used, even though they are actually released as anions, which may or may not be co-transported with H+.

Factors influencing the persistence of organic anions in soil

Much of the debate over the practical importance of organic anions in enhancing the P uptake of plants grown in soil revolves around their persistence in the soil solution. For example, the more carboxyl groups in the organic anion, the more effective it is in increasing the amount of P in solution. At the same time, the more carboxyl groups, the greater the likelihood the organic anion will become bound to the soil surface. Jones and Brassington (1998) found that >80% of the added organic anions (either malate, citrate, or oxalate added at 0.25-5 [micro]mol/g soil) became bound to the soil surface within 10 min. They therefore concluded that this binding would greatly diminish the effectiveness of the organic anions to mobilise nutrients from the rhizosphere. As discussed earlier, the ability of polycarboxylate anions to form soluble complexes with metals sequestered from P adsorbing hydrous oxide surfaces is probably the most important factor determining the extent of P solubilisation (Kirk 1999).

Another consideration is that organic acids can be rapidly consumed by soil microflora. Studies on the mineralisation of exudates in non-rhizosphere soil have shown that organic anions, such as citrate and malate, added at realistic rhizosphere concentrations (10-100 gm) have an average half-life of 2-3 h depending on soil type (Jones and Darrah 1994; Jones et al. 1996b). In general, decomposition rates of organic anions are 2-3-fold faster in rhizosphere soil than in non-rhizosphere soil (Jones 1998). Furthermore, organic acids are only effective at mobilising P from some soils. Jones and Darrah (1994) found that citrate mobilised P from only 1 out of 7 soils. The soil in which P was mobilised had a high Ca-P fraction; even then, only [approximately equal to] 0.03 [micro]moles of P were mobilised per [micro]mole of citrate added.

In contrast, Kirk (1999) used a model, which accounted for the binding of citrate to the soil surface and rhizosphere degradation, to show that observed rates of citrate release from upland rice roots were sufficient to explain P uptake that could not be accounted for by diffusion of readily-available P.

The apparent disagreements in the literature about the effectiveness of root exudates at mobilising soil P are probably because the rhizosphere conditions are highly variable, and depend on a wide range of factors, including soil type, plant species, the microbial species present and their activity, water content, plant nutrition, soil temperature, and weather conditions. Despite the uncertainty caused by our inability to measure root exudation in situ, there appear to be no mechanisms other than chelation of metal ions from hydrous oxide P-adsorbing surfaces that can explain the extensive depletion of NaOH extractable P from moderately and strongly weathered soils (Hedley et al. 1994; Trolove et al. 1996; Zoysa et al. 1998). Indirect evidence continues to be published. Koyama et al. (2000) introduced the gene for mitochondrial citrate synthase into Arabidopsis thaliana, resulting in up to 2.5 times more citrate released from the roots. The additional citrate released resulted in a 27-45% increase in plant rosette diameter and a 26-37% increase in the P content of transformed Arabidopsis leaves compared with non-transformed and wild-type lines when the plants were grown for 4 weeks on a non-allophanic Andosol.

Rhizosphere mobilisation of organic P

Observations of the depletion of organic P in rhizosphere studies are less consistent. For example, Tarafdar and Jungk (1987) found a decrease in organic P in the rhizosphere of wheat and clover, which was significantly correlated with phosphatase activity. Other studies found a small (Gahoonia and Nielsen 1992), or negligible (Trolove et al. 1996) depletion of organic P in the rhizosphere, or even an increase (Hedley et al. 1982b; Zoysa et al. 1999; Chen et al. 2002). Using a Sri Lankan Ultisol, Zoysa et al. (1998) measured significant depletion of NaOH-extractable inorganic and organic P in the rhizosphere of Guinea grass, Calliandra, and bean, but only significant depletion of NaOH-extractable inorganic P in the rhizosphere of tea. The Guinea grass (Calliandra) and bean plants suffered more P stress than the tea plants, but no measures were taken that could explain these differences in organic P mobilisation between plant species. It could be expected that chelating organic anions could also be responsible for organic P release from organo-metallic P complexes in soils. It is likely, however, that a suite of hydrolytic extracellular enzymes (including lignases, lipases, etc.) released by rhizosphere microflora are responsible for breaking organic matter down into low molecular weight compounds from which the more simple phosphatases can cleave the phosphate ester bond P (Chen et al. 2002). One theory that requires testing is that soluble organic P complexes mobilised in the rhizosphere can also diffuse towards the root surface, where the enzymatic hydrolysis of organic P complexes occurs.

Evidence for the direct role of phosphatases in organic P hydrolysis is clouded by the fact that increased phosphatase activity in the rhizosphere is an inducible response to low P status (Hedley et al. 1982b, 1983). Certainly, monoesterases and diesterases have a role as the 'finish' in releasing plant-available P ([H.sub.2]P[O.sub.4-] and HP[[O.sub.4].sup.2-]) from organic matter. Phosphatase activity depends on plant age, plant species, and soil type (Tarafdar and Jungk 1987), and shows an increase as rhizosphere Pi concentrations decrease (Hedley et al. 1982b, 1983, 1994). The study by Hedley et al. (1994) on upland rice grown in an Ultisol showed an increase in phosphatase activity next to the root surface, relative to the bulk soil. However, this increase in phosphatase activity did not correspond to a depletion of organic P in the rhizosphere. The authors therefore concluded that the mobilisation of organic P is not necessarily indicated by increased phosphatase activity. The amount of phosphatase activity measured in moles of P released per hour per weight of rhizosphere soil always exceeds the rate of Pi release, indicating its reaction rate is substrate-limited.

Association with mycorrhizal fungi

Mycorrhizae are formed with the roots of most vascular plants, taking the form of ectomycorrhizae (characterised by dense mycelial sheaths around the roots and intercellular hyphal invasion of the root cortex), which are mostly limited to temperate forest trees, or endomycorrhizae (characterised by external hyphal networks in the soil and extensive growth of arbuscles (and commonly vesicles) within the root cortex cells of the host), which are formed by nearly all other plants. It has been well documented that both forms of mycorrhizae contribute to plant P uptake (see reviews by Bolan 1991; Vogt et al. 1991; Clark and Zeto 2000), and can increase P uptake from sparingly soluble Fe-P (Bolan et al. 1987).

A number of studies have fractionated soil P to investigate whether there are differences between species of mycorrhiza-forming fungi, and mycorrhizal and non-mycorrhizal plants, in their ability to access different P pools (e.g. Li et al. 1991). Sainz and Arines (1988a, 1988b) observed differences in the amount of depletion of the inorganic P fractions between different species of mycorrhizal fungi, suggesting that the endophytes differ in their ability to take up P. To investigate whether mycorrhizal hyphae could access P from different pools to the host plant Li et al. (1991) conducted a rhizosphere study in which only root hairs and mycorrhizal hyphae could explore a soil volume isolated using a 30-[micro]m mesh to exclude roots and a 0.45-[micro]m cellulose acetate membrane to exclude hyphae. These authors demonstrated clearly that a zone of P depletion for mycorrhizal roots extends for the length of the hyphal network away from the rhizoplane (Fig. 9). The soil P depletion profiles for water-soluble (Fig. 9) and 0.5 M NaHC[O.sub.3]-soluble soil P at the 30-[micro]m mesh (boundary for root and root hair) and at the 0.45-[micro]m membrane (boundary for fungal hyphae) were similar in extent and gradient. Li et al. (1991) concluded that hyphae have mechanisms of P uptake similar to plants (i.e. the P absorbing power of hyphae and roots are similar). It should be noted, however, that the experiment of Li et al. (1991) was conducted with a fertilised soil of high P status (initial Olsen P value approx. 80 mg P/kg soil). In their experiment, Li et al. (1991) attributed some of the 'hyphosphere' P depletion to acid production by the hyphal network probably caused by N[[H.sub.4].sup.+] uptake. Whether this W efflux from hyphae was accompanied by organic acid efflux was not measured. In the literature, the question of whether AM hyphae are able to solubilise soil P that is otherwise unavailable to the plant remains a matter of debate; however, the majority of evidence indicates that they are not (Tinker and Nye 2000). In experiments with plants grown in [sup.32]P-labelled soil, the specific activity of P in colonised and uncolonised plants is generally found to be the same, indicating that both plants are accessing P from the same isotopic pools (Tinker and Nye 2000). Li et al. (1991) also showed that both mycorrhizal and non-mycorrhizal plants decreased the concentration of inorganic P in soil but did not affect the concentration of organic P. In contrast, a study by Tarafdar and Marschner (1994) showed a large depletion of organic P by AM hyphae, and Koide and Kabir (2000) clearly demonstrated the ability of the mycorrhizal fungus Glomus intraradices to hydrolyse organic P. Thus, mycorrhizal studies show a similar variation in whether organic P can be solubilised, as do the studies on plant roots (see earlier discussion). The variation in results may be due to soil type, species of mycorrhizal fungi and host plant, and plant age. Certainly, the reasons for these differences warrant further investigation.

[FIGURE 9 OMITTED]

Mycorrhizae increase plant P uptake by more thorough exploration of the soil volume than by roots alone, thereby making 'positionally unavailable' nutrients 'available' (Fig. 10). The extensive hyphal growth of mycorrhizae increases the surface area for absorption and hyphal-transport of P to the host root, which effectively 'short-circuits' the distance for diffusion and stops the P from entering into sorption/desorption reactions with the hydrous Fe- and Al-oxide surfaces of soil particles. Thus, P uptake is accelerated. Further, the diameter of hyphae of mycorrhizal fungi is much finer than that of roots. The fineness of hyphae has two advantages. Firstly, it increases the surface area of hyphae for greater absorption of nutrients. Secondly, it enables the entry of hyphae into pores in soils and organic matter that cannot be entered by roots, thereby increasing the area of exploration (Fig. 10). It has been observed that in both soils and solution cultures, mycorrhizal roots absorbed P almost twice as fast as non-mycorrhizal plants, which has been attributed primarily to the higher affinity and lower threshold concentration of P for absorption by mycorrhizal than non-mycorrhizal plants.

[FIGURE 10 OMITTED]

As with plant roots, organic anion release from mycorrhizal hyphae may also be a factor in soil-P solubilisation. There is evidence that in the case of ectomycorrhizal colonisation of pines, most of the chemical change in the rhizosphere is brought about by organic acid production by the mycorrhizal roots (Cromack et al. 1979; Malajczuk and Cromack 1982; Lapeyrie 1988). Lapeyrie et al. (1987) showed considerable production of oxalate from mycorrhizal hyphae. As mentioned earlier, oxalate is one of the more effective organic acids at releasing P from hydrous Fe- and Al-oxide surfaces.

Reports in the literature suggest that AM are less effective for improving the P uptake by plant species that already have fine root systems. For example, Howeler et al. (1987) found no response of fine-rooted, upland rice to AM inoculation at a range of soil P concentrations and concluded that AM were much more important for coarse rooted species, such as cassava (Manihot esculenta). In contrast, however, other authors have reported greater P uptake of mycorrhizal than of non-mycorrhizal upland rice plants (Sanni 1976; Gangopadhay and Das 1982; Sharma et al. 1988; Pradhan and Mohan 1996). Such contrasts in the literature probably indicate that there is a range of conditions under which mycorrhizae provide increased P uptake, whether they be the degree of colonisation or the nutrient status of the soil and these conditions vary between experiments. Soil conditions may create a low level of inoculum. Inoculum levels are often low if the rice is planted after a flooded crop (Ilag et al. 1987), or after a long period of unplanted fallow (Thompson 1991). Also, the rate of root colonisation by AM can be slow. Abbott and Robson (1982) found that AM colonisation of subterranean clover (Trifolium subterraneum) took at least 2 weeks, and more than 6 weeks for some other plant species.

Mycorrhizal research on upland and flooded rice is important in the context of providing technology to improve the P uptake efficiency of staple food crops grown on marginal soils of the tropics and subtropics. Increases in grain yield of flooded rice as a result of mycorrhizal colonisation have been reported in both pot (Sivaprasad et al. 1990; Secilia and Bagyaraj 1992; Solaiman and Hirata 1996, 1997) and field trials (Iqbal et al. 1978; Ortiz and Fernandez 1998). However, a yield decrease due to AM colonisation was observed in one treatment in a study by Solaiman and Hirata (1995). Generally, these increases in grain yield have been in the order of 10-30%. Secilia and Bagyaraj (1992) obtained 15-20% increase in rice grain yield in AM inoculated treatments compared with the non-inoculated control, which had received twice the amount of P fertiliser. The observed increases in grain yield were generally attributed to an increase in the uptake of P, and increases in N and trace element uptake were also observed in some studies. Arbuscular mycorrhizae might, therefore, be beneficial to P uptake in rice. The benefits of mycorrhizae are likely to increase in situations where the initial amount of inoculum in the soil is high, e.g. following an upland crop or pasture.

Howeler et al. (1987) found that crop responsiveness to mycorrhizal inoculation is highly dependent on a number of factors: the species and strain of mycorrhizal fungi inoculated, the effectiveness of the mycorrhizae already present in the soil, soil P, N, and K status, soil pH, soil temperature, and soil moisture. The differences between the results of Howeler et al. (1987) and the other researchers listed in the above paragraph highlights the fact that more research needs to be done in order to understand the benefit of mycorrhizae to rice under upland and rainfed conditions. The results of Howeler et al. (1987), however, highlighted that upland rice is more P efficient than various other tropical crops, and that rice is not responsive to mycorrhizal colonisation in comparison with them. It seems important, therefore, to elucidate the mechanism of P efficiency in rice.

Comments on rhizosphere methodologies

Most of the evidence for rhizosphere P depletion has been obtained by growing plants in thin layers of soil, root study containers, or the similar rhizobox technique. Root study container (Fig. 5) and thin layer techniques (Fig. 2) are useful to confine and enhance the rhizosphere effect such that soil chemical changes can be observed experimentally. The size of the root mass generating the P sink strength and the amount of root-released acidity are factors to be considered in interpreting the results obtained. For example, in the experiments conducted by Trolove et al. (1996) growth of 3 white clover genotypes and lotus was poor on unfertilised soil with an Olsen P status of 11 mg P/kg soil and insufficient soil P was taken up at the planar rhizosphere for P fractions to be depleted by measurable amounts. When the soil was fertilised with MCP or reactive PR, plant growth increased, as did the root mass at the planar rhizosphere, and there was measurable depletion of soil P forms. Lotus plants produced greater shoot and root mass than the clover plants and caused greater rhizosphere acidification and higher P uptake per plant. The uptake of soil P per unit root length, however, was greater for the clover genotypes. Thus, whilst the root study containers allowed rhizosphere soil samples to be taken to demonstrate the P solubilising processes, more depletion of the soil P fractions by the Lotus was not a consequence of greater P solubilisation per root length.

[FIGURE 2-5 OMITTED]

Increasing the root mass at the constrained, planar-rhizosphere generates more acidity to diffuse into the soil layers below the mesh. Thus, poor plant growth on unfertilised soil may generate insufficient acid and insufficient P demand for P fractions in unfertilised soils to be depleted by measurable amounts (Trolove et al. 1996). It is therefore important to measure the root length generating acidity, organic anion, and/or enzyme activity in order to quantify the significance of the observation.

Do we need more rhizosphere research?

A number of studies (reviewed above) have demonstrated that rhizosphere biochemistry can be manipulated by roots and mycorrhizal hyphae such that various soil-P forms can be solubilised and taken up by the host plant. The significance of the biochemical change (H+, organic anion excretion, or extracellular enzyme synthesis) in effecting soil-P release will vary as the nature of soil P varies. Polycarboxylic anion excretion may be more effective than H+ excretion at effecting P release for plants growing in moderately to strongly weathered soils, containing P mostly associated with hydrous oxides of Fe and Al. Do we know if such organic anion excretion is commonplace in plants adapted to growth in strongly weathered soils? This is one of the areas in which further research could improve our understanding of the distribution of such mechanisms in the plant world.

Some P-efficient cultivars have already been identified amongst crop plant species and bred for the purpose of high yield on soils with adequate plant-available P. Should we look again at some of the native and wild species that grow in very low P status soils?

If we are to introduce P-efficient species or cultivars to our current farming systems, multidisciplinary efforts are required to integrate land management techniques (cultural sensitivity included), soils, fertiliser, and P-efficient cultivars into crop production packages that will lead to more sustainable food production. A major issue is that many P-efficient cultivars compromise on yield or seed quality.

In the depths of the rhizosphere science, improved techniques are required to study roots in vivo, particularly for measuring either the low concentrations of organic acids released into in soil solution, or the temporal nature of that release and subsequent solubilisation of soil-P. On the analytical side, recent progress involves the use of capillary electrophoresis (Barbas et al. 1999; Xu et al. 2002), ion chromatography (Tani et al. 2001), and ion exclusion chromatography (Fischer 2001), which allows detection of the nanomolar concentrations of organic anions likely released from small sections of growing root per day.

We also need to revisit the whole area of organic P movement in the rhizosphere to assist our understanding of P transport processes to roots and reasons for the observed organic P depletion in some studies but not others.

We can also report that 'rhizosphere science' is alive and well--watch out for new publications in the next 50 years. In particular, an exciting new area is phytomining research (Anderson et al. 1998) and 'rhizosphere bioremediation' of contaminated soils. Researchers are finding that the rhizosphere, with its elevated microbial activity and increased concentrations of organic anions, has improved abilities to detoxify soils containing heavy metals (Dutton and Evans1996; Russell et al. 2000) and, perhaps, contaminating organics, such as polychlorinated biphenyls.
Table 1. The pH and concentrations (mmol/kg soil) of organic anions
extracted from thin-layers of unplanted soil and rhizosphere soil of
98-day-old Lotus pedunculatus (Bolan et al. 1997)

Two soils were used: Ramiha (allophanic) and Halcombe
(derived from siliceous loess)

Soil treatment pH Acetate Citrate Lactate

 Ramiha
Unplanted 5.6 0.33 0.07 0.15
Rhizosphere 4.9 2.50 0.67 1.51
 Halcombe
Unplanted 5.4 0.33 0.33 0.33
Rhizosphere 4.8 1.59 0.39 1.16
1.s.d. (P = 0.05) 0.38 0.14 0.06 0.08

Soil treatment Malate Oxalate Formate

Unplanted 0.19 traces traces
Rhizosphere 3.66 0.64 12.20

Unplanted 0.33 0.33 0.33
Rhizosphere 1.21 0.28 2.23
1.s.d. (P = 0.05) 0.08 0.06 0.35

Table 2. Average composition (mg/g fresh root, with range in
parentheses) of root exudates from four lowland rice cultivars
(Lin and You 1989)

Sugar Av. amount Organic anion Av. amount

Fructose 6.7 (3.4-9.3) Citrate 0.9 (0.4-1.8)
Sucrose 5.5 (9.8-1.0) Malate 0.6 (0.2-1.0)
Glucose 0.5 (0.0-1.0) Succinate 0.5 (0.0-1.2)
 Lactate 0.3 (0.0-0.5)

Sugar Amino acids Av. amount

Fructose Basic 1.3 (0.9-1.7)
Sucrose Other 1.2 (1.1-1.3)
Glucose


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Manuscript received 11 October 2002, accepted 14 February 2003

S. N. Trolove (A,B), M. J. Hedley (A,D), G. J. D. Kirk (C), N. S. Bolan (A), and P. Loganathan (A)

(A) Soil and Earth Sciences, Institute of Natural Resources, Massey University, Private Bag 11222, Palmerston North, New Zealand.

(B) Present address: The New Zealand Institute for Crop and Food Research Ltd, PO Box 85, Hastings, New Zealand.

(C) Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, Cambridge, England.

(D) Corresponding author; email: m.hedley@massey.ac.nz
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Author:Trolove, S.N.; Hedley, M.J.; Kirk, G. J. D.; Bolan, N. S.; Loganathan, P.
Publication:Australian Journal of Soil Research
Date:May 1, 2003
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