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Environmental and Experimental Botany 69 (2010) 267–272

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journa l homepage: www.e lsev ier .com/ locate /envexpbot

otton, wheat and white lupin differ in phosphorus acquisitionrom sparingly soluble sources

iaojuan Wanga,c, Caixian Tanga,∗, Chris N. Guppyb,c, Peter W.G. Salea

Department of Agriculture Science, La Trobe University, Bundoora, VIC 3086, AustraliaSchool of Environmental and Rural Science, University of New England, Armidale, NSW 2351, AustraliaCotton Catchment Communities CRC, Locked Bag 1001, Narrabri, NSW 2390, Australia

r t i c l e i n f o

rticle history:eceived 20 October 2009eceived in revised form 9 April 2010ccepted 13 April 2010

eywords:

a b s t r a c t

Low responsiveness of cotton to P fertilizer application on soils with low soil-test P values indicates thatcotton might take up P from stable P pools. The ability of cotton to acquire P from sparingly soluble Psources was examined by comparing with wheat and white lupin. The plants were grown in washed riversand, with P sources applied at a rate of 40 mg P kg−1, as sparingly soluble AlPO4, FePO4, or hydroxya-patite. Cotton was inefficient in accessing P from any of the sparingly soluble P sources. Thus, the low

lPO4

uptakehizosphere pHhizosphere exchangeable Aloot Al accumulation

responsiveness of cotton to P fertilizers could be attributed to factors other than efficient P acquisitionfrom the stable P pool in the soil. In contrast to white lupin which accessed little P from the sparinglysoluble P sources in this study, wheat showed an outstanding ability in utilizing AlPO4. When comparedwith the control, total uptake of P from AlPO4 by wheat was approximately 9 times higher than cottonand 7 times higher than white lupin, which was possibly related to its high root Al concentration andhigh root:shoot ratio. The study concludes that the three species differed substantially in P acquisition

e AlP

from the sparingly solubl

. Introduction

Inorganic phosphorous (P) in the soil is mainly bound to eitheralcium (Ca) in calcareous soils or iron (Fe) and aluminium (Al) incid soils, reducing availability to plants (Hinsinger, 2001). Applica-ion of soluble P fertilizers is frequently required to achieve optimalield. However, soluble P once applied is often quickly fixed by Ca,e or Al in the soil, mainly as precipitates of low solubility and lowlant-availability. Thus, a large proportion of soil P is in stable andnavailable forms. When P supply is inadequate, the replenishingf soil solution P from these stable pools would mainly depend onlant-induced P solubilisation.

Chemical processes in the rhizosphere that are responsible for Polubilising-activity include exudation of proton or hydroxyl ions,nd organic anions (Hinsinger, 2001). Diversity in root responseso P deficiency is reflected in differing abilities of plant species toccess P from sparingly soluble P forms. For example, Zhang et al.1997) found that P-starved radish utilized P from Al phosphate effi-

iently when tartaric acid was detected as the major form of organiccid exuded. Buckwheat and rape are well recognized for their highapacity for proton release and thus were efficient in taking up Prom alkaline soils (Mclachlan, 1976). Ae et al. (1990) reported that

∗ Corresponding author. Tel.: +61 3 9479 2184; fax: +61 3 9471 0224.E-mail address: C.Tang@latrobe.edu.au (C. Tang).

098-8472/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.envexpbot.2010.04.007

O4, with cotton being least efficient and wheat most efficient.© 2010 Elsevier B.V. All rights reserved.

pigeon pea is more efficient in utilizing Fe phosphate than cerealsand other leguminous crops due to the release of piscidic acid fromroots.

Knowledge on species’ ability in utilizing various sparingly sol-uble P sources would help understanding of P uptake behavior ofthe crop under field conditions. However, such information is lack-ing for the cotton plant, the major crop species in eastern-northernAustralian farming systems. Low responsiveness of cotton to P fer-tilizers on alkaline soils with low soil-test P values (Bronson et al.,2001; Dorahy et al., 2004) might indicate that cotton uses P mainlyfrom stable pools rather than from soluble P sources. Further evi-dence is provided by the strong correlation between the soil Al–Pand Fe–P fractions and P uptake of cotton plants at early flower-ing under field conditions (Dorahy et al., 2004). Although previousresearch revealed that cotton plants depleted little P from stableP pools in the soil that associated with Ca (Wang et al., 2008), therelative availability of P bound with Al and Fe to cotton still remainsunknown.

The aim of this study is to investigate the ability of cotton toaccess P from sparingly soluble P sources, such as AlPO4 (Al–P),FePO4 (Fe–P), and hydroxyapatite (Ca10–P), when compared with

wheat and white lupin. Wheat is considered a physiologically ineffi-cient P-acquiring species (Nuruzzaman et al., 2005), whereas whitelupin is an efficient species due to known organic acid release(Gardner et al., 1983). We hypothesized that the low responsive-ness of cotton to P fertilizer application on soils with low soil-test

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68 X. Wang et al. / Environmental and

values is due to its efficiency in acquiring sparingly soluble Pources. The study used wheat and lupin as comparison species,nd was undertaken in washed sand to facilitate the measurementf root access to P supplied in the different sparingly soluble forms.

. Materials and methods

.1. Experiment design and plant culture

The experiment consisted of six P treatments, three crop speciesnd three replicates. The six P treatments include zero P (P0) andve P sources supplied as KH2PO4 (K–P), Ca(H2PO4)2 (Ca–P), AlPO4Al–P), FePO4 (Fe–P), and hydroxyapatite (Ca10–P). K–P and Ca–Pre water-soluble P sources while Al–P, Fe–P and Ca10–P representhe main form of sparingly soluble P in acid soils and alkaline soils,espectively.

Plants were grown in 3.5 kg of coarse river sand (<2 mm). Theoarse river sand had the following chemical properties: pH 5.80.01 M CaCl2), total C 0.55 mg kg−1, total N 0.03 mg kg−1, avail-ble P 2.6 mg kg−1 and exchangeable Al 0.12 mg kg−1 (1 M KCl).asal nutrients were mixed with the river sand at the follow-

ng rates (mg kg−1): K2SO4, 140; CaCl2·2H2O, 150; MgSO4·7H2O,0; MnSO4·H2O, 15; ZnSO4·7H2O, 9; CuSO4·5H2O, 2; H3BO3, 0.7;a2MoO4·2H2O, 0.2; FeEDTA, 5.5. Nitrogen was applied weekly atrate of 30 mg N kg−1 as Ca(NO3)2 to each pot after planting. Phos-horus sources were added as powder at a rate of 40 mg P kg−1

oil to the designated treatment soils. Potassium was balanced forhe treatment K–P. The soil (sand) was then mixed thoroughly withasal nutrients and P, and weighed into a PVC tube (10 cm diameter,0 cm high) lined with plastic bags.

Cotton (Gossypium hirsutum L. cv. Sicala 60 BR), wheat (Triticumestivum L. cv. Yitpi) and white lupin (Lupinus albus L. cv. Kiev)ere planted in a glasshouse with a diurnal temperature range

f 16–30 ◦C. Uniform germinated seeds were sown at a depth ofcm. Seed P content was determined as 0.54, 0.18 and 1.00 mg Per seed for cotton, wheat and white lupin, respectively. One weekfter sowing, plants of wheat, cotton and white lupin were thinnedo 6, 2 and 2 per pot, respectively, to keep similar biomass. Theots were watered to 80% of field capacity every 2 days for the firstweeks, and then daily for the final 3 weeks. In order to mini-ize the leaching effect during watering, water was supplied via a

mall tube (i.d. 6 mm) with outlet holes below the top 5 cm downo 30 cm.

.2. Plant and rhizosphere sand measurement

Plants were harvested 40 days after sowing when the appar-nt treatment effect in terms of shoot biomass growth was visual.efore harvesting, the moisture of the coarse river sand was

ntentionally maintained at about 60% field capacity, the optimaloisture level tested for the collection of rhizosphere sand. After

utting the plastic bags into half, plants were lifted up and shakenently to remove the bulk sand from the roots. Sand that remaineddhered to the roots was considered rhizosphere sand, and col-ected by shaking them off the roots after further drying.

Soil available P (Olsen P) and exchangeable Al (1 M KCl) waseasured for both rhizosphere sand and bulk sand according to

he method described by Olsen and Dean (1965) and Conyerst al. (1991), respectively. The activity of acid phosphatase wasetermined by measuring the release of para-nitrophenol from

ara-nitrophenyl phosphate following exposure to soil in a mod-

fied universal buffer (MUB) at pH 6.5 as described by Tabatabaind Bremner (1969). The pH was measured using a Thermo Orion20 pH meter after extraction in 0.01 M CaCl2 solution (1:5 (w/v)oil:solution ratio) by shaking for 17 h on an end-over-end shaker.

mental Botany 69 (2010) 267–272

Shoots were cut off above the soil surface, washed and weighed.All roots were carefully collected, washed with deionized waterand weighed. Cluster roots on the white lupin were counted andrecorded. Both plant shoots and roots were dried at 70 ◦C for 48 h,weighed and ground. Subsamples were digested with concentratednitric and perchloric acid (4:1) for determination of P, K, Ca, Aland Fe using ICP-AES (Inductively Coupled Plasma Atomic Emis-sion Spectrometry). Total Al and Fe concentrations determined inthe entire root would represent Al and Fe in both root symplasmand all apoplastic pools.

2.3. Statistical analysis

All data were subjected to two-way ANOVA, followed by themultiple comparisons with the least significant difference usingGenstat (11th version) for windows. Checks for normal distribu-tion of the data, and for homogeneity of variance, found that no datatransformations were required. Means are presented with standarderrors.

3. Results

3.1. Plant growth

Application of soluble K–P and Ca–P increased shoot and rootdry weights of wheat and cotton significantly when compared witheither control or less soluble P sources treatments (Fig. 1). Wheatobtained the maximum shoot dry weight with P supplied as K–Pwhile cotton accumulated the most shoot biomass when suppliedsoluble Ca–P. Shoot and root dry weights of white lupin did notshow significant response to any supplied P source.

Species variation in P acquisition from the sparingly soluble Psources can be expressed in relation to the response to soluble Psources. Wheat showed the highest relative P efficiency when sup-plied as Al–P (0.56) (relative to soluble P), followed by cotton (0.21).However, relative P efficiency in accessing P from Fe–P and Ca10–Pwas low for both wheat (0.07, 0.07) and cotton (0.03, 0.11). Severeleaf senescence was observed 3 weeks after planting in wheat with-out P supply or supplied with Fe–P or Ca10–P. Application of solubleP sources significantly suppressed cluster root formation in whitelupin compared with no P supply, and most root clusters were pro-duced in the treatments with P supplied as Fe–P and Ca10–P (datanot shown). Nodules on the white lupin were virtually absent dueto regular N supply.

Regardless of P sources, the root/shoot ratio of wheat was 2–3times higher than that of cotton and white lupin (p < 0.05) (Fig. 1).The root/shoot ratio of both wheat and cotton was greatest whenP was not supplied, decreased by 15% when supplied with spar-ingly soluble P forms, and 30% when supplied with soluble P.However, the root/shoot ratio of white lupin was not affected byP treatment.

3.2. Plant P concentration and uptake

The concentration of P in the shoot and root, and total P uptakewas highest in K–P and Ca–P treatments for all species (Fig. 2). Withapplication of any sparingly soluble P sources, cotton showed nosignificant increase in P concentrations compared with the no Pcontrol. However, the addition of Al–P increased P concentration

compared with P0 (p < 0.05). When compared with P0, total Puptake from Al–P by wheat was approximately 9 times higherthan cotton and 7 times higher than white lupin (p < 0.05) (Fig. 2).Total P uptake from Fe–P and Ca10–P was less significant for allspecies.

X. Wang et al. / Environmental and Experimental Botany 69 (2010) 267–272 269

Fig. 1. Total shoot and root dry weights and root:shoot ratio of wheat, cotton and white lupin grown for 40 days with zero P (P0) or 40 mg kg−1 P as KH2PO4 (K–P), Ca(H2PO4)2

(Ca–P), AlPO4 (Al–P), FePO4 (Fe–P), and hydroxyaptite (Ca10–P). Error bars indicate the standard error (n = 3). The main effects of species and P treatment and their interactionwere significant (p < 0.001). For each panel, the LSD (p = 0.05) is also presented for the species × P treatment interaction.

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ig. 2. The concentration of P in shoot and root, and total P uptake of wheat, cottolPO4 (Al–P), FePO4 (Fe–P), and hydroxyaptite (Ca10–P). Error bars indicate the stanignificant (p < 0.001). For each panel, the LSD (p = 0.05) is also presented for the spe

.3. Concentrations of K, Ca, Fe and Al in plant

Concentrations of K and Fe in shoot and root of all species wereot affected by P source. A dilution effect of biomass production onhoot Al concentration of cotton and root Al concentration of wheatas detected when P was applied as soluble K–P and Ca–P (Table 1).

he concentration of K was much higher in shoot of wheat thanotton and white lupin, while the opposite was observed for thehoot Ca concentration (p < 0.05). Application of Ca–P resulted in aignificantly higher level of Ca accumulated in the shoot of cottonnd white lupin, compared with other P sources. When averagedver the P treatments, Al concentration in roots of wheat was 2.5nd 4 times higher than that of cotton and white lupin, respectivelyp < 0.05).

.4. Rhizosphere pH, acid phosphatase, exchangeable Al andvailable P

Irrespective of P source or plant species, pH was invariablyigher in the rhizosphere than in the bulk sand (Fig. 3). For wheat,hizosphere pH was higher when supplied with soluble P sources

nd Al–P (p < 0.05). Similarly, the rhizosphere pH of cotton wasighest when supplied with soluble sources also (p < 0.05). The

ncrease in the rhizosphere pH did not vary among the P treat-ents for white lupin. Bulk soil pH was increased in all P sources

or wheat and in soluble P sources for cotton.

white lupin supplied with zero P (P0), and P as KH2PO4 (K–P), Ca(H2PO4)2 (Ca–P),error (n = 3). The main effects of species and P treatment and their interaction wereP treatment interaction.

The activity of acid phosphatases increased in the rhizosphereof all species when compared with the bulk soil. The activity was20–30% higher in wheat, and 100–150% higher in white lupin whenP was not applied or applied with the sparingly soluble P thanwhen soluble P was applied (p < 0.05). In comparison, only P0 andAl–P resulted in an increased acid phosphatase activity in the rhi-zosphere of cotton.

When P was applied as sparingly soluble P sources, available Pin the rhizosphere did not vary among the treatments or amongspecies (Fig. 4). Species supplied with soluble P sources had avail-able P of more than 20 mg kg−1 in the rhizosphere at harvesting.There was no difference among the P treatments in exchangeableAl in the rhizosphere of cotton and white lupin (Fig. 4). However,exchangeable Al in the rhizosphere sand of wheat increased from<0.1 mg kg−1 in the zero P treatment to 0.8, 0.6 and 1.1 mg kg−1 inthe treatments of K–P, Ca–P and Al–P, respectively (p < 0.05).

4. Discussion

This study showed that the three species differed substantiallyin P acquisition from sparingly soluble P sources, in particular from

Al–P. It also revealed, for the first time, that cotton lacks the abil-ity to access P from sparingly soluble P sources. Thus the lowresponsiveness of cotton to P fertilizer application on soils withlow soil-test P values is unlikely to be attributed to the efficientuse of P from sparingly soluble P pools in soil. Although wheat

270 X. Wang et al. / Environmental and Experimental Botany 69 (2010) 267–272

Table 1Concentration of K, Ca, Fe and Al in shoot and root of wheat, cotton and white lupin supplied with zero P (P0), KH2PO4 (K–P), Ca(H2PO4)2 (Ca–P), AlPO4 (Al–P), FePO4 (Fe–P),and hydroxyapatite (Ca10–P).

Crop species Treatment K concentration Ca concentration Fe concentration Al concentration

Shoot Root Shoot Root Shoot Root Shoot Root

(mg g−1) (mg g−1) (mg g−1) (mg g−1)

Wheat P0 46.9 21.6 7.3 3.4 0.075 2.90 0.087 2.35K–P 50.1 19.4 6.4 7.7 0.089 3.20 0.060 1.74Ca–P 49.3 18.8 6.9 9.2 0.087 2.77 0.068 1.97Al–P 48.9 18.1 7.4 5.9 0.084 2.88 0.059 2.48Fe–P 50.5 23.6 7.7 3.5 0.098 2.74 0.077 2.56Ca10–P 50.8 22.2 7.6 4.0 0.082 2.65 0.069 2.48

Cotton P0 28.5 17.3 18.3 6.9 0.103 1.24 0.087 0.98K–P 37.0 20.6 20.6 7.6 0.092 1.27 0.056 0.61Ca–P 33.8 20.7 22.6 9.1 0.087 1.20 0.056 0.58Al–P 32.6 18.9 18.7 6.6 0.101 1.02 0.080 0.86Fe–P 30.4 18.3 18.0 6.5 0.131 1.12 0.071 0.85Ca10–P 32.2 19.1 20.0 6.4 0.095 1.00 0.068 0.81

White lupin P0 31.6 35.8 17.2 13.0 0.373 2.48 0.091 0.58K–P 39.2 38.3 20.9 13.8 0.387 3.14 0.070 0.63Ca–P 31.6 32.4 23.2 16.3 0.336 2.52 0.069 0.63Al–P 32.4 33.9 18.7 15.4 0.388 2.64 0.068 0.59Fe–P 33.3 36.2 17.6 16.1 0.356 2.92 0.072 0.59Ca10–P 31.6 35.9 17.4 14.8 0.333 2.46 0.067 0.52

LSD (p = 0.05) for any two means 8.7 6.2 2.4 3.7 0.046 0.69 0.033 0.50Crop species *** *** *** *** *** *** n.s. ***

P treatment n.s. n.s. *** *** n.s. n.s. ** *

Specie × P n.s. n.s. *** * n.s. n.s. n.s. *

n.s., not significant.* p ≤ 0.05.

** p < 0.01.*** p < 0.001

Fig. 3. The pH and acid phosphatase activity of rhizosphere and bulk sand of wheat, cotton and white lupin supplied with zero P (P0), and P as KH2PO4 (K–P), Ca(H2PO4)2

(Ca–P), AlPO4 (Al–P), FePO4 (Fe–P), and hydroxyapatite (Ca10–P). Error bars indicate the standard error (n = 3). The main effects of species and P treatment and their interactionwere significant for rhizosphere pH, bulk pH and acid phosphatase activity in rhizosphere soil (p < 0.001). For each panel, the LSD (p = 0.05) is also presented for the species × Ptreatment interaction. The dotted line represents the original pH of the growth medium. n.s., not significant.

X. Wang et al. / Environmental and Experimental Botany 69 (2010) 267–272 271

Fig. 4. Concentrations of available P and exchangeable Al in the rhizosphere soil of wheat, cotton and white lupin supplied with zero P (P0), and P as KH2PO4 (K–P), Ca(H2PO4)2

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Ca–P), AlPO4 (Al–P), FePO4 (Fe–P), and hydroxyapatite (Ca10–P). Error bars indicaheir interaction were significant for rhizosphere available P (p < 0.05) and exchangreatment interaction. The dotted line represents the original available P and excha

s considered to be a P-inefficient species, it could access P froml–P better than white lupin, a P-efficient species. The findings areonsistent with another study on species’ ability in using sparinglyoluble P sources in three soils using a 32P reverse dilution tech-ique (Wang, 2009). The following discussion will focus on theseifferential species responses to sparingly soluble P sources andhy these results were observed.

Among all the sparingly soluble P sources tested, cotton accessedittle P from Al–P and was completely unable to use Fe–P anda10–P. The observed tissue P concentrations (∼1.2 mg g−1) wereelow the critical values reported for cotton (2.0–3.1 mg g−1) (Coxnd Barnes, 2002; Crozier et al., 2004). This is consistent with previ-us findings that physiological traits, such as release of carboxylateshich would allow plants to access sparingly soluble forms of P,ere not detected for the cotton plant under P-deficient conditions

Wang et al., 2008). In addition, the lower availability of Ca10–P tootton in this study is consistent with the negligible depletion ofcid-extractable P (mainly P bound with Ca) pools in the rhizo-phere soil of cotton (Wang et al., 2008). While Dorahy et al. (2004)ound a strong correlation between P uptake by cotton and the Al-nd Fe–P fractions in soil from a field experiment, these pools inertosols represent P weakly adsorbed to Al and Fe oxides (Soilsnd Torrent, 1989). Precipitation of P with Al and Fe rarely occursn alkaline soils (Lindsay et al., 1962). Thus, if the low responsive-ess of cotton to P fertilizer application on soils with low soil-test Palues indicates that cotton plants are able to meet their P require-ent from soil P pools, these pools would represent P that are

elatively plant-available but not measured by the standard bicar-onate extraction procedure.

The observed pH increase in the rhizosphere, when comparedith bulk sand, could be due to the excess uptake of anions, mainlyO3

−, over cations and subsequently release of OH− ions from rootsHinsinger et al., 2003), since N was supplied as Ca(NO3)2. The rhi-osphere pH remained below that which would be observed in theolution of Vertosol soils commonly used to grow cotton and wheatn northern-eastern Australia. Higher rhizosphere pH was invari-bly detected for the treatments that achieved higher biomassesponse. This is attributed to greater NO3

− uptake and assimilationnder conditions of better shoot and root growth with sufficientsupply. Since the mobilization of P from Ca10–P was generally

ssociated with the acidification of the rhizosphere (Bertrand et al.,999; Hinsinger and Gilkes, 1996), dissolution of P from Ca10–Pay be greatly hampered by the release of OH− ions and thus was

ess effective to all species in our study. However, the dramaticncrease in rhizosphere pH was attributed to the poor pH buffer-

standard error (n = 3). The main effects of species and P treatment (p < 0.001) andAl (p < 0.001). For each panel, the LSD (p = 0.05) is also presented for the species × Ple Al of the original sand medium.

ing of coarse river sand, and should not be used as an indication ofstrong alkalinisation of the rhizosphere under field conditions.

An exceptional ability of wheat to access P from Al–P wasobserved in this study. This accords with recent observations byPearse et al. (2006, 2007). However, mechanisms responsible forthis efficient use of Al–P in wheat remain unclear. Ample evi-dence exists that Al toxicity could induce a release of di- andtri-carboxylates from wheat roots due to activation of an anionchannel by Al (Ryan et al., 1997, 2001). Nevertheless, the rhizo-sphere pH detected in this study was too high (>6) to induce Altoxicity. Pearse et al. (2006) found that wheat was superior inusing Al–P despite releasing few carboxylates into its rhizosphere.Thus, the role of carboxylates in mobilizing Al–P by wheat remainsunclarified and warrants further research.

Alternatively, release of OH− following NO3− assimilation

would facilitate Al–P (Ksp = 6.3 × 10−19) dissolution due to the for-mation of less soluble Al(OH)3 (Ksp = 4.6 × 10−33). However, if thisis the case, cotton and white lupin should be similarly efficient inusing Al–P. In addition, the pH increase in the rhizosphere of wheatfed with Al–P might indicate that OH− consumed for Al–P dissolu-tion was less significant. It appears that mechanisms involved in theefficiency of wheat in utilizing Al–P are independent of increasedrhizosphere pH.

On the other hand, considering that sparingly soluble Al–Pincreased availability with prolonged incubation (Wang, 2009),wheat, with higher root:shoot ratio than both cotton and whitelupin, could possibly be better equipped to acquire this progres-sively available P source. The higher accumulation of Al in the rootof wheat than cotton and white lupin (Table 1) might further drivethe reaction towards the dissolution of Al–P. At pH above 6.3, solu-ble Al species in the rhizosphere of wheat exists almost exclusivelyas Al(OH)4

− (Davis and Hem, 1989; Ma et al., 2003). Directly orindirectly, Al(OH)4

− has to be accumulated by wheat root into itsapoplastic, cell wall or mucilage (Archambault et al., 1996; Zhenget al., 2004), to account for the high root Al concentrations mea-sured, but minimize the risk of Al toxicity. Solubility of Al(OH)4

−

increases towards more alkaline conditions (Ma et al., 2003), whichsubsequently explains why increased exchangeable Al was onlydetected in the rhizosphere of wheat fed with K–P, Ca–P and Al–Pthat demonstrated the highest rhizosphere pH.

Surprisingly, white lupin was not superior in using any sparinglysoluble P sources. In a similar study, Pearse et al. (2006, 2007) alsorevealed a poor performance of white lupin in accessing sparinglysoluble P sources. These results are apparently in contradiction withthe reported high efficiency of white lupin in P mobilization from

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he soil. We propose the following explanations. First, the largeeed size of white lupin delayed the onset of P deficiency, andacquisition strategies were not displayed in our studies due to

he short duration of the experiment. For example, Bolland andrennan (2008) found that seed size and P content could markedlyffect the P utilization of white lupin for shoot biomass produc-ion, and shoot yield showed no response to applied P at the earlyrowth stage (e.g. 51 days after sowing). Second, release of rootxudates does not always relate consistently to a crop species’bility to use P precipitated with Al, Fe or Ca (Tang et al., 2007;earse et al., 2007). Pearse et al. (2006) attributed the poor per-ormance of white lupin in using Al–P to the rhizosphere soil pHhich did not favour the complexation reactions between exuded

arboxylates and metals (Pearse et al., 2006). Third, the increasedhizosphere pH in our study could hinder the normal functioning ofhe white lupin which is sensitive to alkaline pH (Tang et al., 1993).inally, the large increase in acid phosphatase activity in the rhi-osphere of white lupin supplied with sparingly soluble P sourcesay provide an indication that part of the efficiency of white lupin

n acquiring P under field conditions is related to the mobiliza-ion of organic P sources. The potential benefit of increased acidhosphatase in the rhizosphere in acquiring soil organic P could beubstantial (George et al., 2006), although its direct effect could note evaluated in this study due to negligible organic P in the sandedium.In conclusion, the species varied greatly in their ability to take up

from sparingly soluble P forms Al–P, Fe–P and Ca10–P. This speciesariation could not be explained by the difference in their root exu-ation (Wang et al., 2008). Cotton lacked the ability to access all ofhese P sources, in contrast to the high efficiency of wheat in Al–Pcquisition. Thus possible strategies, which allow cotton to acquirefrom the soil and become less responsive to P fertilizer applica-

ion, would include its efficient use of organic P (Wang et al., 2008;ang, 2009), access to P in the subsoil through its deep root sys-

ems (Singh et al., 2005; Wang, 2009) and mycorrhizal associationDuggan et al., 2008; McGee et al., 1997). White lupin did not dis-lay a high efficiency in the utilization of sparingly soluble P sources

n this study and some other studies. Its efficiency in P acquisitionppears to be greatly affected by soil pH, form of N supplied, geno-ype, P sources and seed P reserve. While the majority of previoustudies used simple growth media (e.g. solution culture) or singleoils, direct associations between root exudation and P-use effi-iency of white lupin covering a wide range of soils deserve furthernvestigation. The high efficiency of wheat to use Al–P might beelated to its extensive root system and great ability to bind Al inhe root. These should be explored in future studies, consideringhat wheat is widely grown in soils containing significant amountsf Al–P.

cknowledgements

We thank La Trobe University, and Cotton Research and Devel-pment Corporation for financial support.

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