Influence of phosphorus and biofertilizers on soybean and wheat root growth and properties

Field Crops Research xxx (2014) xxx–xxx

G ModelFIELD 6254 No. of Pages 9

Influence of phosphorus and biofertilizers on soybean and wheat rootgrowth and properties

Dibakar Mahanta a,b,*, Raj K. Rai a, Shiva Dhar Mishra a, Arunkumar Raja b,Tapan J. Purakayastha a, Eldho Varghese c

a Indian Agricultural Research Institute, New Delhi – 110 012, IndiabVivekananda Institute of Hill Agriculture (ICAR), Almora – 263 601, Uttarakhand, Indiac Indian Agricultural Statistical Research Institute, New Delhi – 110 012, India

A R T I C L E I N F O

Article history:Received 15 April 2014Received in revised form 8 June 2014Accepted 9 June 2014Available online xxx

Keywords:Phosphorus inflow rateRoot cation exchange capacityRoot length densitySoybeanVAMWheat

A B S T R A C T

Alteration of crop root morphology is a new innovative approach to provide food security. Phosphorus isthe most important nutrient to influence root properties. Efficient use of P fertilizers has become animportant issue of agriculture all over the world due to limited availability of rock phosphate and its non-renewable nature. Hence, root properties and grain yield of soybean–wheat cropping system wereevaluated by inoculation of phosphate solubilizing bacteria (PSB) and vesicular arbuscular microorgan-ism (VAM) with 50% recommended P (0.5 P + PSB + VAM) against 100% P (1.0 P), 50% P and control in aTypic Ustochrepts of the Indo-Gangetic plains. The root cation exchange capacity (CEC) of soybean andwheat treated with 0.5 P + PSB + VAM were 3.6 and 4.6% higher than 1.0 P, respectively. The sametreatment produced 2.3 and 2.6% higher root length density (RLD) in soybean and wheat, respectively incomparison to 1.0 P. The P inflow rate under 0.5 P + PSB + VAM was 9.2 and 4.6% higher than 1.0 P insoybean and wheat, respectively indicating higher acquisition of P through VAM, although higherrhizospheric P availability was recorded in 1.0 P. The root CEC, RLD and P inflow rate were closely relatedto P concentration and content in root, shoot and nodule, specific root length, root diameter and internal Prequirement. The better root property observed in 0.5 P + PSB + VAM enhanced 4.1 and 4.9% grain yield ofsoybean and wheat, respectively as compared to 1.0 P. Inoculation of PSB and VAM could substitute 50% Pof soybean–wheat cropping system with better root property and higher grain yield in semi-arid subtropics of the Indo-Gangetic plains.

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1. Introduction

Phosphorus (P) may be present in relatively large amounts, butmuch of it is poorly available because of the very low solubility(Smith et al., 2011) and fixation of soluble P. It is generally acceptedthat the mechanism of mineral phosphate solubilization by PSBstrains is associated with the release of low molecular weightorganic acids, which through their hydroxyl and carboxyl groupschelate the cations bound to phosphate, thereby converting it intosoluble forms (Chen et al., 2006; Panhwar et al., 2011). Furthervesicular arbuscular mycorrhizas (VAM) grow extensively in soil to

* Corresponding author at: Vivekananda Institute of Hill Agriculture (ICAR),Almora – 263 601, Uttarakhand, India. Tel.: +91 5962 241005; fax: +91 5962 241250.

E-mail addresses: [email protected] (D. Mahanta),[email protected] (R.K. Rai), [email protected] (S.D. Mishra),[email protected] (A. Raja), [email protected] (T.J. Purakayastha),[email protected] (E. Varghese).

http://dx.doi.org/10.1016/j.fcr.2014.06.0160378-4290/ã 2014 Published by Elsevier B.V.

Please cite this article in press as: Mahanta, D., et al., Influence of phoproperties, Field Crops Res. (2014), http://dx.doi.org/10.1016/j.fcr.2014.0

form a well-developed hyphal network that absorbs inorganicphosphate several centimeters away from the root surface. P istranslocated rapidly to the roots overcoming the slow diffusionthat occurs in the soil solution. The individual fungal hyphae havemuch smaller diameters than roots, allowing access to narrowersoil pores and hence increasing the soil volume explored andproviding a larger surface area for absorption (Smith et al., 2011).VAM are also able to take P from soil solution with low phosphateconcentration, where simple roots have difficulties in tapping theions (Bolan, 1991). VAM-inducible plant PiT genes are expressedexclusively in the colonized cortical cells, which are involved in theuptake of Pi released. Additionally, H+-ATPases energize the plantplasma membrane surrounding the intracellular fungal structures,facilitating active Pi uptake (Smith et al., 2011). The high effectivityof VAM in phosphorus uptake is not only caused by their smalldiameter and large surface area, but also the accumulation ofpolyphosphates in their vacuoles where it serves storage functionsand in terms of energy as an alternative to ATP. Polyphosphates are

sphorus and biofertilizers on soybean and wheat root growth and6.016

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presumably also involved in transport of phosphate in the hyphaeto the infected root where it is hydrolyzed in the arbuscules andmost likely transported as inorganic phosphate across the plasmamembrane of the host root cell. Polyphosphates are stronglynegative polyanions and also serve important functions in thecation/anion balance of the fungus, and by binding cations such asmagnesium, potassium and basic amino acids such as arginine andglutamine also as carriers for hyphal transport of these solutes tothe host root cell. The solute transport in the hyphae, other mineralelements and the plasma streaming are the driving force for thistransport (Marschner, 1997).

Phosphate solubilizing bacteria (PSB) and vesicular arbuscularmicroorganisms (VAM) are reported to improve phosphorusnutrients of crop plants (Vance et al., 2003; Yan et al., 2004).However, there is a paucity of information on the individual as wellas combined role of PSB and VAM on root morphology, P inflowrate, root cation exchange capacity and internal phosphorusrequirement with single superphosphate in soybean and wheat.Again, root studies are undertaken less compared to shoot studies,because root sample acquisition and analysis are tedious and timeconsuming (Zoon and Van Tienderen, 1990). Additionally, rootmass, which is easier to measure than total root length, surfacearea and diameter has been used to compare root systems (Murphyand Smucker, 1995), but root mass measurements are notindicative of the total absorptive area of the root system andalteration of root morphology can happen without a change in totalroot biomass (Iman et al., 2006). Plants can dramatically alter theirroot architecture to optimize growth in a large variety of soilnutrient conditions (Den Herder et al., 2010).

The objective of the study was to investigate the individual aswell as combined effects of PSB and VAM along with 50% singlesuperphosphate on root morphology, P inflow rate, root cationexchange capacity and internal P requirement, and yield ofsoybean and wheat. The hypothesis of the study was thatinoculation of PSB and VAM would improve root characteristicsand substitute substantial amount of P fertilizer without sacrificinggrain yield through better acquisition.

2. Materials and methods

The experimental site was situated in Indian AgriculturalResearch Institute (IARI), New Delhi, India (latitude: 28� 380 N,longitude: 77� 090 E and altitude: 229 m above mean sea level). Ithas a semiarid, subtropical climate with hot dry summers and coldwinters. The mean maximum temperature during the hottestmonth of July is about 38.9 �C, while the mean minimumtemperature in the coldest month of January is as low as 6.3 �C.The annual average temperature is 24.3 �C. The normal onsetperiod of monsoon is in the third week of June. The mean annualrainfall is 614 mm, three-fourth of which is received during July–September and the remaining one-fourth between October andJune. The soil of the farm belongs to order Inceptisol, Mahauliseries. The soil is sandy loam in texture, well levelled, deeppercolating and well drained, hypothermic family of the TypicUstochrept (old alluvium). The soil was having the followingcharacteristics in 0–15 cm depth: pH 8.36 (1:2.5 soil:watersuspension), easily oxidizable (K2Cr2O7 + H2SO4) organic C 5.8 gkg�1, alkaline KMnO4 oxidizable N 66.7 mg kg�1, 0.5 M NaHCO3

extractable P 6.2 mg kg�1 and 1.0 N NH4OAc exchangeable K62.6 mg kg�1 soil.

The experiment was conducted for two years, which includedtwo crops per year, soybean (July–October) and wheat (November–April) with seven phosphorus (P) management practices, viz, 1.0 P{recommended dose of P (RDP) through single superphosphate},phosphate solubilizing bacteria (PSB) + Vesicular arbuscular my-corrhiza (VAM), 0.5 P (half the RDP), 0.5 P + PSB, 0.5 P + VAM, 0.5


P + PSB + VAM, and control (without P). The RDP for soybean andwheat were 34.9 and 26.2 kg P ha�1, respectively, which wereapplied through single superphosphate (6.99% water-soluble P).The inoculum species used for PSB and VAM were Pseudomonasstriata and Glomus fasciculatum, respectively and were obtainedfrom the Division of Microbiology, IARI, New Delhi. The PSB wasinoculated at the rate of 500 g carrier ha�1 and the populationcount was 100,000,000 cells g�1 of the carrier. VAM was applied as5 kg carrier (soil) ha�1 and the spore count was 30 spores g�1

carrier. Single superphosphate was applied as per the requirementof treatment. Bradyrhizobium japonicum inoculant was commonfor all the treatments in soybean. The recommended doses of N(30 kg N ha�1 for soybean and 120 kg N ha�1 for wheat) and K(33.2 kg ha�1 for both soybean and wheat) were applied uniformlyto all the plots. Fertilizers used were urea (46% N) for N and muriateof potash (KCl-50% K) for K. The treatments were distributed in arandomized block design with three replications in a fixed plot ofsize 5 m � 4.5 m.

Soybean genotype “PK 1042” and wheat genotype “HD 2643”were used as seed for experimentation and were released byGBPUAT, Pantnagar and IARI, New Delhi, respectively. These twogenotypes are released for commercial cultivation in North Plainzone of India, where the experiment was conducted at IARI, NewDelhi is situated. Soybean was sown (80 kg seeds ha�1) in the thirdweek of July each year. The seeds were manually sown in rows45 cm apart at a depth of about 5 cm. After seeding, a light rollerwas dragged to cover the seeds. Full doses of N, P and K wereincorporated before sowing. Hand weeding was also done tomanage the weeds and plant protection measures were applied asneeded to control the diseases and pests. Crops were harvestedmanually 5 cm above the ground at physiological maturity in thesecond week of October using sickles. After soybean harvest, wheatwas sown in the third and fourth week of November in the first andsecond year, respectively. Wheat was sown by hand (100 kgseeds ha�1) in rows 22.5 cm apart to a depth of about 5 cm. Handweeding was also done to manage the weeds. Wheat washarvested at 5 cm above the soil surface in the fourth week ofApril and straw was removed from the plots. Both the crops werecultivated under irrigated conditions.

2.1. Root studies

Root studies with respect to root length and root diameter werecarried out during both the years in two stages i.e. at 40 and 80 daysafter sowing (DAS) for soybean and 45 and 90 DAS for wheat crop.These days were chosen for crops, because the second samplingcoincided with flowering stage of respective crops and by that timemaximumgrowth of roots had takenplace. After the harvest of aboveground plant parts, root samples were collected using root samplingcore (15 cm height, 8 cm diameter). Five root sampling cores wereused in each plot on each sampling date. The sampling tube wascentered over the plant and a sample was taken to a 15 cm depth.These cores were immersed in water to disperse the soil. The rootswere obtained by gradually loosening the soil. The remaining soiladhered to roots were washed properly by putting roots on thecontainer with sieves of several mesh sizes to prevent loss of fineroots during washing, following the method of Costa et al. (2000).Each sample was placed in a plastic, sealable bag. Roots wereimmediately taken tothe laboratoryandkept intherefrigeratorsetat4 �C till analysis. Then these root samples were dried in oven at 70 �Cuntil constant weight and the dry weight was recorded.

2.1.1. Root length and average diameterRoot length and average diameter were measured using a

Hewelett Packard scanner controlled by Win-RHIZO Programme V.



Table 1Effect of phosphorus and biofertilizers on grain yield of soybean and wheat (mean oftwo years).

Treatment Mean grain yield (t ha�1)

Soybean Wheat

1.0 P 2.00 4.30PSB + VAM 1.69 3.890.5 P 1.78 3.970.5 P + PSB 1.87 4.100.5 P + VAM 1.95 4.360.5 P + PSB + VAM 2.09 4.51Control 1.17 3.21LSD (P = 0.05) 0.14 0.15

D. Mahanta et al. / Field Crops Research xxx (2014) xxx–xxx 3


2002C Software (Regent Instruments Inc. Ltd., Quebec, Canada).Here roots were placed in the plexiglas tray (200 mm � 300 mm)with 4–10 mm deep water layer, depending on root size. Rootswere spread on the tray before scanning to minimize overlapping.After scanning, the analysis of the image was done by theprogramme itself. After scanning, root samples were oven-dried todetermine dry weight.

2.1.2. Root length density (RLD)Root length density was calculated as the ratio of the root length

(RL, cm) to the root sample core volume (V, cm3) (Myers et al.,2007)

RLD cmcm�3� � ¼ RLV

(1)

2.1.3. Relative root growth constantRelative root growth constant expresses the root length

increase in a time interval in relation to the initial root lengthand can be estimated from the following formula (Fohse et al.,1991):

Relative root growth constant k; cmcm�1day�1� �

¼ lnRL2 � lnRL1t2 � t1

(2)

where, RL is root length, t is time and the subscripts refer to the firstand second observation.

2.1.4. Specific root length (SRL)Specific root length (SRL) is probably the most commonly

measured morphological parameter of fine roots because it isbelieved to characterize the economic aspects of root systems. SRLis the length-to mass ratio of a root fragment (Ostonen et al., 2007).

Specific root length SRL; m=gð Þ ¼ Root length RLð ÞRoot dry weight RootWð Þ (3)

2.1.5. Root CECThe root samples at flower initiation stage were powdered,

sieved through 1 mm sieve and cation exchange capacity of rootwas then determined by adding HCl to ground root and washingthrough KCl, which was titrated back to neutral pH (7.0) by KOH(Crooke, 1964).

2.1.6. Phosphorus inflows (I)Phosphorus inflow into the roots during the two inter-sampling

periods (40–80 DAS and 45–90 DAS for soybean and wheat,respectively) was calculated by the following formula (Jakobsenet al., 1992):

I ¼ðP2�P1Þ �ln RL2

RL1

� �

ðt2�t1Þ � ðRL2�RL1Þ (4)

where, P refers to total amount of P in plant, t to plant age and RL toroot length. The subscripts refer to the first and secondobservations of respective crops.

2.1.7. Internal phosphorus requirement (IPR)Internal phosphorus requirement during the two inter-sam-

pling periods (40–80 DAS and 45–90 DAS for soybean and wheat,respectively) was calculated by the following formula:

IPR ¼ ðP2�P1ÞðShoot W2� Shoot W1Þ (5)

where, P refers to total amount of P in plant and Shoot W to shootdry weight. The subscripts refer to the first and secondobservations of respective crops.


For most plants, the concentration of the absorbing roots isgreatest in the upper part of the root zone and near the base of theplant. The distribution of active roots in a normal soil isapproximately triangular in shape, the greatest concentrationbeing near the soil surface. The usual extraction pattern shows thatabout 40% of comes from the upper quarter of the root zone, 30%from the second quarter, 20% from the third quarter and 10% fromthe bottom quarter. The root zone depth of soybean and wheat are90 and 120 cm, respectively (Reddi and Reddy, 1997). The total P,SRL, relative root growth constant, P uptake per root dry weight, Puptake per root length and P inflow rate were estimated byconverting from 15 cm root depth under direct observationbetween 120 and 90 cm for soybean and wheat, respectively withconsideration of four quarters of the root zone for secondobservation.

2.2. Rhizosphere soil

The root system, together with adhering soil was carefullyremoved from the soil. Then shaking of the root system was done toremove the bulk soil and only the soil that is removed bysubsequent brushing was considered as rhizosphere soil (Lusteret al., 2009). Then the rhizospheric soil pH (1:2.5 soil:watersuspension) and available P (0.5 M NaHCO3 extractable P) wereestimated.

2.3. Statistical analysis

Statistical analysis of the data was done using ANOVA techniqueand following SPSS 10.0 and SAS 9.2 software. The treatmentmeans were compared at P < 0.05 level of probability for workingout LSD values.

3. Results

The grain yield of soybean and wheat was increased signifi-cantly due to the application of phosphorus and biofertilizers(Table 1). The highest grain yield was obtained with the applicationof 50% P along with inoculation of phosphate solubilizing bacteria(PSB) and vesicular arbuscular mycorrhiza (VAM) (0.5 P + PSB +VAM) in both soybean and wheat crop. The increase in grain yieldwith 0.5 P + PSB + VAM over application of 100% P (1.0 P) were 4.1and 4.9% for soybean and wheat crop, respectively. The grain yieldfor soybean under 0.5 P + PSB + VAM, 1.0 P and 0.5 P + VAM plotswere statistically non-significant to each other. But, in case ofwheat, the grain yield under 1.0 P plots was significantly lower than0.5 P + PSB + VAM plots. The grain yield under 0.5 P + PSB + VAM and0.5 P + VAM were at par to each other and the treatments fordecreasing grain yield sequence were 0.5 P + PSB + VAM followedby 0.5 P + VAM and 1.0 P in wheat. There was no interactionbetween treatment and year for grain yield and other rootparameters.



Table 2Effect of phosphorus and biofertilizers on P concentration and content of root and shoot at different stages of soybean and wheat (mean of two years).

Treatment P concentration (mg g�1) P content (mg plant�1)

Soybean Wheat Soybean Wheat

40 DAS Flowering 45 DAS Flowering 40 DAS Flowering 45 DAS Flowering

Root Shoot Root Shoot Nodule Root Shoot Root Shoot Root Shoot Root Shoot Nodule Root Shoot Root Shoot

1.0 P 3.98 4.18 3.83 3.59 5.12 2.10 3.79 1.90 3.35 2.17 24.9 28.1 117 4.42 0.289 0.924 3.88 17.5PSB + VAM 3.47 3.67 3.12 3.02 4.26 1.71 3.35 1.51 2.94 1.42 16.1 18.6 69 2.71 0.195 0.510 2.48 13.00.5 P 3.61 3.93 3.35 3.15 4.52 1.85 3.49 1.62 3.05 1.67 18.7 21.0 75 3.21 0.225 0.594 2.81 14.20.5 P + PSB 3.80 4.04 3.51 3.35 4.72 1.91 3.61 1.75 3.15 1.83 21.6 23.4 91 3.71 0.246 0.716 3.25 15.40.5 P + VAM 3.88 4.10 3.64 3.48 4.88 2.00 3.74 1.93 3.39 2.00 23.0 25.1 103 4.01 0.286 0.874 4.02 18.20.5 P + PSB + VAM 4.03 4.26 3.87 3.69 5.16 2.18 3.90 1.99 3.46 2.32 26.5 29.1 127 4.63 0.325 1.030 4.30 19.6Control 2.94 3.10 2.59 2.61 3.80 1.43 2.80 1.07 2.36 0.86 8.8 13.1 47 1.46 0.111 0.257 1.30 6.5LSD (P = 0.05) 0.13 0.09 0.07 0.10 0.07 0.06 0.12 0.06 0.23 0.16 2.6 0.6 8 0.32 0.021 0.079 0.17 1.5



The highest root P concentration at flower initiation stage wasobserved under 0.5 P + PSB + VAM plots (3.87 and 1.99 mg g�1 forsoybean and wheat, respectively) for both soybean and wheatcrops, which was 0.04 and 0.09 m g g�1 higher than 1.0 P plots insoybean and wheat crops, respectively (Table 2). Similar trendswere also recorded for P concentration in shoot of both crops,nodule of soybean and P content in both crops in different stages.Although the rhizospheric available P status under 1.0 plots weresignificantly higher than 0.5 P + PSB + VAM plots, the P concentra-tion and content in different plant parts were lower in 1.0 plotsthan the later. Inoculation of VAM enhanced 5–14 and 23–44% Pconcentration and content, respectively in different plant parts anddifferent stages of observation.

The specific root length (SRL) in soybean crop was non-significant among different treatments (Table 3). But there wassignificant decrease of SRL in wheat with application of phospho-rus and inoculation of biofertilizers. The lowest SRL of wheat cropwas recorded under 0.5 P + PSB +VAM plots (7.64 m g�1), which was0.36 and 1.10 m g�1 lower than 1.0 P and control plots, respectively.The relative root growth constant (RGR) significantly increased insoybean, while it decreased in wheat, with P fertilizer andbiofertilizer inoculation. Inoculation of both the biofertilizers with0.5 P (0.087 cm cm�1 day�1) enhanced 5% RGR of soybean crop ascompared to 1.0 P plots, while it (0.054 cm cm�1 day�1) was 5%lower in wheat crop.

The root diameter under control plots were the thinnest(0.494 mm) in soybean crop, while there was no significantdifference for root diameter in wheat crop. Application of differentphosphorus levels and inoculation of different bio-fertilizers andtheir combinations significantly enhanced cation exchange capac-ity (CEC) of roots in both soybean and wheat crops. The root CEC ofplots inoculated with both PSB and VAM to 0.5 P were 0.8 and0.7 cmol kg�1 higher in soybean and wheat, respectively ascompared to the roots under 1.0 P plots.

Table 3Influence of phosphorus and biofertilizers on root growth and properties of soybean a

Treatment Specific root length (m g�1) atflower initiation stage

Relative root growth constant

day�1) at flower initiation stag


1.0 P 6.91 8.00 0.083 0.057

PSB + VAM 6.84 8.44 0.073 0.058

0.5 P 6.79 8.44 0.077 0.058

0.5 P + PSB 6.72 8.15 0.080 0.058

0.5 P + VAM 6.88 7.79 0.083 0.056

0.5 P + PSB + VAM 6.91 7.64 0.087 0.054

Control 6.75 8.74 0.062 0.063

LSD (P = 0.05) NS 0.44 0.003 0.004


The root length density (RLD) of soybean and wheat wasincreased significantly with the application of phosphorus andbiofertilizers. The RLD under 0.5 P + PSB + VAM plots (0.856 and0.363 cm cm�3 in soybean and wheat, respectively) (Fig. 1),provided 2.3 and 2.6% higher in soybean and wheat, respectivelythan 1.0 P plots. The phosphorus inflow rate (2.29 mg P m�1 rootday�1and 0.747 mg P m�1 root day�1 for soybean and wheat,respectively) through root in plots treated with 0.5 P + PSB + VAMwere 0.193 and 0.033 mg P m�1 root day�1 higher than 1.0 P plots insoybean and wheat, respectively. The internal P requirement of 0.5P + PSB + VAM plots (4.68 and 4.18 mg P g�1 above ground biomassin soybean and wheat, respectively) were 0.08 and 0.13 mg P g�1

above ground biomass higher than 1.0 P plots for soybean andwheat crop, respectively.

Inoculation with PSB + VAM had the lowest soil pH (7.06 and7.35 for soybean and wheat, respectively) at flower initiation stageof both the crops (Table 4). It was followed by control (for soybeancrop only �7.23) and 0.5 P + PSB (7.60 and 7.46 for soybean andwheat) plots. The rhizosphere soil pH at the flower initiation stagewas highest in soils under application of 1.0 P plots in both crops.The highest rhizospheric available P at flower initiation stage wasrecorded under 1.0 P plots in both crops. Among the reduced levelof P application and inoculation of biofertilizers, 0.5 P + PSB + VAMrecorded the highest available P during flower initiation stage.

A correlation matrix (Table 5) showed significant correlations(P < 0.05) between all the different root and soil parameters andgrain yields of soybean and wheat, except SRL in soybean and soilpH in wheat. This indicated that soil pH had negligible role for grainyield, root morphology and other characteristics of wheat andsimilarly SRL in case of soybean. The RLD and root CEC were instrong correlation with P inflow rate, internal P requirement andrelative root growth constant.

The contrast analysis in Table 6 indicated that P andbiofertilizers play a very important role for improving root

nd wheat (mean of two years).

(cm cm�1

eAverage rootdiameter (mm) at flowerinitiation stage

Root CEC (cmol kg�1 root dry weight)at flower initiation stage


0.522 0.573 23.2 15.20.490 0.577 19.2 13.10.511 0.581 19.8 13.00.519 0.577 22.5 13.90.520 0.578 22.8 15.70.521 0.580 24.0 15.90.494 0.606 15.2 8.10.020 NS 0.7 0.8



Fig. 1. Root length density, phosphorus inflow rate and internal phosphorus requirement (mean of two years) at flower initiation stage of soybean and wheat under differentphosphorus management practices (RLD = root length density; P inflow rate = mean P inflow rate of crop between 40/45 DAS and flower initiation stage; IPR = mean internal Prequirement of crop between 40/45 DAS and flower initiation stage; 1.0 P = 100% recommended dose of P; 0.5 P = 50% recommended dose of P; PSB = phosphate solubilizingbacteria; VAM = vesicular arbuscular mycorrhiza). Error bars represent standard deviation.



characteristics and grain yield of soybean and wheat, especiallysoybean (control vs rest). It is clearly proved from the contrastanalysis of 0.5 P vs 0.5 P + BF and 1.0 P vs 0.5 P + BF (Table 6) thatbiofertilizers (PSB and VAM) are inevitable for P fertilization insoybean and wheat crops. Inoculation VAM played more importantrole than PSB with 50% recommended P for grain yield and rootcharacteristics as indicated from the lower probability in 0.5 P vs0.5 P + VAM than 0.5 P vs 0.5 P + PSB (Table 6). The high probability(P > 0.05) in the contrast analysis of all root parameters and grainyield for 1.0 P vs 0.5 P + PSB + VAM indicated that inoculation ofboth PSB and VAM with 0.5 P substituted 50% of recommended P.

Root CEC and RLD were found to be two of the most importantparameters influencing other root properties and grain yield(Table 5). It is clearly indicated from the correlation coefficients ofroot CEC and RLD with grain yield, P inflow rate and IPR (Table 5).Near perfect linear relationship of P inflow rate and grain yieldwith root CEC and RLD showed that differences in theseparameters were associated with differences in root CEC and RLD.

4. Discussion

The yield was improved in the treatment 0.5 P + PSB + VAM,compared to 1.0 P. The increase in grain yield might have been dueto increase in P concentration and content in root, shoot andnodule (Table 2). The near perfect linear relationship of grainyield with shoot P concentration showed that differences in yieldwere associated with differences in shoot P concentration (Fig. 2).It indicated that P acquisition is more important as compared toits higher application rate to enhance productivity of crops. Theaction of PSB is not only the release of plant available P, but rather

Table 4Effect of phosphorus and biofertilizers on soil pH and available P at flower initiation s

Treatment Rhizosphere soil pH at flower initiation stage

Soybean Wheat

1.0 P 7.97 7.66

PSB + VAM 7.06 7.35

0.5 P 7.67 7.65

0.5 P + PSB 7.60 7.46

0.5 P + VAM 7.81 7.70

0.5 P + PSB + VAM 7.73 7.50

Control 7.23 7.73

LSD (P = 0.05) 0.16 0.07


through the production of plant growth promoting and biologi-cally active substances like indole acetic acid, gibberellins andcytokinin (Mahanta, 2008), which might have enhanced produc-tivity. Similarly, VAM are widely recognized to improve plantacquisition of P by enhancing translocation and transfer ofphosphate ions from the soil solution to the root cells and finallythe uptake (Vance et al., 2003; Yan et al., 2004). Again, VAMresponds to lower threshold concentration of P for absorptionthan do plant roots (Bolan, 1991). Further PSB was stimulated inthe root zone of the VAM inoculated plants (Barea and Azcon-Aguilar, 1983), which altogether increased the productivity with0.5 P + PSB + VAM in comparison to 1.0 P plots. The ability of aninoculated PSB to supply P to a plant may be limited; eitherbecause the compounds released by PSB to solubilize phosphateare rapidly degraded or because the solubilized phosphate is re-fixed before it reaches the root surface. This is the reason ofrelatively lower probability in grain yield and root properties(Table 6), for contrast analysis of 0.5 P vs 0.5 P + VAM as comparedto 0.5 P vs 0.5 P + PSB. However, if the phosphate released by PSBis taken up by a mycorrhizal mycelium, the result would be a co-operative synergistic microbial interaction that improved Pacquisition by the plant (Barea et al., 2005). Hence, inoculationof PSB and VAM substituted 50% of P application and similarresults have been reported by Tanwar et al. (2013). The increasesin grain yields from 0.5 P + PSB + VAM plots were 78 and 40% forsoybean and wheat, respectively as compared to the control plots.This clearly demonstrates the importance of P nutrition tosoybean crop than wheat.

The combination of P with VAM proved superior to P with PSBin both the crops as indicated from productivity (Table 1) and

tage of soybean and wheat (mean of two years).

Rhizosphere available P (mg kg�1) at flower initiation stage

Soybean Wheat

45.5 35.211.9 11.819.9 19.630.6 28.925.8 25.431.7 29.84.6 4.64.7 3.5



Table 5Correlation between grain yield of soybean and wheat and root properties.

SY/WY RLD Dia Root age CEC pH P Inflow IPR SRL RGR

SoyabeanSY 1.000 0.960*** 0.811* �0.998*** 0.979*** 0.731 0.836* 0.932** 0.986*** 0.632 0.990***

RLD 1.000 0.857* �0.958*** 0.970*** 0.802* 0.894** 0.991*** 0.988*** 0.723 0.974***

Dia 1.000 �0.837* 0.872** 0.948*** 0.876** 0.871* 0.874** 0.372 0.863*

Root age 1.000 �0.983*** �0.752 �0.832* �0.936** �0.988*** �0.610 �0.995***

CEC 1.000 0.766* 0.876** 0.963*** 0.992*** 0.586 0.988***

pH 1.000 0.858* 0.797* 0.800* 0.459 0.777*

P 1.000 0.870* 0.887** 0.503 0.838*

Inflow 1.000 0.974*** 0.704 0.962***

IPR 1.000 0.649 0.994***

SRL 1.000 0.630RGR 1.000WheatWY 1.000 0.993*** �0. 841* 0.980*** 0.992*** �0.224 0.883** 0.996*** 0.995*** �0.938** �0.973***

RLD 1.000 �0.877** 0.958*** 0.992*** �0.199 0.900** 0.998*** 0.994*** �0.907** �0.948***

Dia 1.000 �0.772* �0.891** 0.462 �0.760* -0.880** -0.829* 0.630 0.794*

Root age 1.000 0. 964*** �0.248 0.788* 0.968*** 0.962*** �0.936** �0.995***

CEC 1.000 �0.268 0.859* 0.995*** 0.986*** �0.908** �0.962***

pH 1.000 �0.053 �0.244 �0.143 0.080 0.321P 1.000 0.888** 0.910** �0.827* �0.769*

Inflow 1.000 0.992*** �0.909** �0.963***

IPR 1.000 �0.943*** �0.948***

SRL 1.000 0.912**

RGR 1.000

SY: soybean grain yield; WY: wheat grain yield; RLD: root length density at flowering stage of crop; Dia: root diameter at flowering stage of crop; root age: mean root age; CEC:root CEC at flowering stage of crop; pH: rhizosphere soil pH at flowering stage of crop; P: rhizosphere soil available P status at flowering stage of crop; inflow: P inflow rate;IPR: internal P requirement; SRL: specific root length at flowering stage of crop; RGR: relative root growth constant.

* Indicate significance at 5% level.** Indicate significance at 1% level.*** Indicate significance at 0.1% level.



probability level of significance for contrast analysis (Table 6). Theaddition of VAM along with PSB increased the effect beyond thatobserved from the addition of either micro-organism alone in boththe crops (Tables 1 and 6). However, PSB inoculated alone with Pdid not increase the yield significantly, perhaps because thepresence of already available form of P that might have decreasedthe performance of PSB.

Inoculation of PSB and VAM coupled with 0.5 P enhanced Pconcentration and content in root, shoot and nodule (Uddin et al.,2014) in comparison to 1.0 P application with higher P flowthrough the root from soil and ultimately enhanced P acquisitionthrough higher root CEC, RLD, P inflow rate, root foraging and soil Pmining capacity (Richardson et al., 2011). It clearly indicated thatPSB and VAM mobilized more P to the plant from soil. Thecompatibility of P and VAM can be attributed to the fact that thevesicular arbuscular mycorrhiza might be instrumental in mobi-lizing soluble P and might have increased the surface area ofabsorption through hyphae, thus availability of nutrients frominaccessible areas. VAM increase P uptake by more throughexploration of soil volume thereby making ‘positionally unavail-able’ nutrients ‘available’. This is achieved by decreasing thedistance for diffusion of phosphate ions and by increasing the

Table 6Probability level of significance for contrast analysis of grain yield, root surface area densinfluence (SRI) of soybean and wheat.

Source Grain yield Root length density


Control vs rest <0.0001 <0.0001 <0.0001 <0.0001

0.5 P vs 0.5 P + BFa 0.0157 0.0016 0.0022 0.0394

1.0 P vs 0.5 P + BF 0.6460 0.8356 0.1200 0.8919

0.5 P vs 0.5 P + PSB 0.3070 0.2923 0.2161 0.4702

0.5 P vs 0.5 P + VAM 0.0689 0.0039 0.0223 0.0387

0.5 P vs 0.5 P + PSB + VAM 0.0022 0.0002 0.0001 0.0237

a BF: it includes individual or combination of biofertilizers i.e. PSB, VAM individually aP + PSB + VAM).


surface area for absorption (Tinker, 1980). The diameter of hyphaeof VAM i.e. 2–4 mm, is less than the diameter of root hairs. Thefineness of hyphae has two fold advantages. Firstly, it increases thesurface area of hyphae for greater absorption of nutrients.Secondly, it enables the entry of hyphae into pores in soils andorganic matter that cannot be entered by root hairs and therebyincreases the area of exploration (Bolan, 1991). Besides, theacquisition of organically bound P is improved by acid phospha-tase, and through hormones released from VAM, which might haveexerted beneficial effect (Tarafdar and Marschener, 1994) on Pconcentration, content in root and shoot of soybean and wheat.

Inoculation of PSB and VAM maintain the growth of roots andcrops as a whole by providing enough phosphorus throughincreasing available P status (Fernández et al., 2007; Sundaraet al., 2002) and acquisition (Smith et al., 2011), respectively.However, application of 1.0 P could not maintain the root length as0.5 P + PSB + VAM, although having highest available P status(Table 4). It might be due to the lack of better acquisition incomparison to later treatment. The root length in wheat is directlyproportional to P nutrition and similar results in maize (Braun-berger et al., 1991) and rice (Panhwar et al., 2011) have beenreported. The RLD is directly proportional to root length and hence

ity, P inflow rate, internal phosphorus requirement (IPR), root age and sphere of root

P inflow rate IPR Root age

Soybean Wheat Soybean Wheat Soybean Wheat

<0.0001 <0.0001 <0.0001 <0.0001 <0.0001 0.00240.0012 0.0925 0.0468 0.0125 0.0002 0.27230.4889 0.9563 0.5898 0.8239 0.9664 0.51570.1218 0.5767 0.3282 0.3834 0.0811 0.95920.0134 0.1191 0.1280 0.0140 0.0019 0.31430.0001 0.0455 0.0172 0.0052 <0.0001 0.1074

nd combination of both PSB + VAM (combination of 0.5 P + PSB, 0.5 P + VAM and 0.5



Fig. 2. Response of shoot P concentration at flowering stage to grain yield of soybean and wheat (shoot P concentration at flowering stage of soybean and wheat with grainyield under respective crops of different phosphorus management practices were taken for this response calculation).



the increase of RLD with inoculation of both biofertilizers with 50%P. The enhancement of RLD with application and better nutrition ofP has been widely reported (Jaidee et al., 2013; Sheng et al., 2012;Suri and Choudhary, 2013; Teng et al., 2013).

Soybean crop at flower initiation stage produced roots with lowaverage diameter in PSB + VAM and control plots, which was due tothe increase in number of root hairs resulted from P deficiency(Caroll et al., 2003). This behaviour of soybean root is justified aslegume roots typically respond to P deficiency through allocationof more carbon to roots, resulting in increased number of root hairs(Jungk et al., 1990). Plants grown under 1.0 P and 0.5 P + PSB + VAMfaced relatively less P deficiency due to high available P and Ptransport through hyphae of VAM, respectively. In wheat root,there was no significant difference between the treatments foraverage root diameter. But in general higher and lower rootdiameter was related to lower and higher P nutrition, respectively(Braunberger et al., 1991).

The P inflow rate depends upon available P concentration inrhizospheric soil and acquisition efficiency of P by the crop. Thehigh inflow rate of both soybean and wheat crops in 1.0 P plotswere obvious due to high rhizospheric P concentration in floweringstage (Table 4). Ironically, 0.5 P + PSB + VAM plots provided higher Pinflow rate than 1.0 P plots, although the available P status werelower (Table 4). Inoculation of PSB and VAM to 0.5 P enhanced rootCEC and RLD and the higher P inflows might have been sustainedthrough the higher P acquisition by the VAM infection (Jones et al.,1998). This improved P uptake per unit root length could be due tofactors of increase in the root surface area per unit root length(Haling et al., 2013). It clearly proved that acquisition andmobilization of P, which was provided by VAM, is more importantthan P availability. The effect of PSB, VAM and PSB + VAM with 0.5 Penhanced 18, 30 and 53% P inflow rate, respectively in soybean and5, 13 and 17%, respectively in wheat crop. Hence, the effect of PSBand VAM on P acquisition in soybean was almost three timeshigher than wheat crop. The term “internal P requirement” can bedefined as the amount of phosphorus required to produce unitabove ground biomass dry weight. The internal requirementgenerally parallels, but is not identical with the “criticalconcentration” and is reflective of available nutrient status of soil.Internal P requirement of soybean and wheat was determined atflowering stage and the values were highest in inoculation withboth biofertilizers and 0.5 P plots for both the crops. Inoculation ofVAM, which helped in mobilizing P more efficiently from soil tocrops, that enhanced the IPR in both the crops treated with 0.5P + PSB + VAM as compared to plots treated with 1.0 P, although thelatter plots had significantly higher rhizospheric available P(Rehman et al., 2005; Sarfraz et al., 2009; Sattar et al., 2011).


It was observed that the root CEC was higher in treatmentswhere P availability was higher (Banerjee, 2005). Inoculation ofVAM further increased the root CEC. The increase in root CECfollowing VAM application by altering root cell structure,particularly at the fungus-cell interface (Bonfante-Fasolo andGianinazzi-Pearson, 1979) through fungus infection. The cyto-plasm of the host cell is separated from the hyphae by an interfacialpectic matrix, altering cell wall structure that might contribute tohigher CEC of VAM inoculated roots (Yang and Goulart, 2000). TheP in the soil may be related to the formation of energy richphosphorylated nitrogen compounds at the outer surface of cellsand these substances may be able to escort cations and anionsacross the protoplast. Thus, an increase in P uptake was associatedwith exchange capacity of root (Banerjee et al., 2010). Better Pavailability increased number as well as length of root hairs whichwere more active and possessed more pectic substance anddirectly increased root CEC (Mahanta, 2008). Thus inoculation ofPSB and VAM to 0.5 P enhanced root CEC than 1.0 P.

Inoculation of PSB enhanced rhizospheric available P. PSB iscapable of forming organic acids which are sources of bioticallygenerated H+ ion and dissolve mineral phosphate and solubilizefixed P and make it available to plant. Sometimes these liberatedacids from unionized association with metal (chelation) andincrease the concentration of soluble phosphate. Thus the PSB isinstrumental in enriching the rhizosphere with greater amount ofavailable P while it lacks mechanisms to deplete it, so the PSBinvolved treatments resulted in greater soil available P inrhizosphere (Banerjee, 2005). Phosphatase production or otherforms of enzymatic hydrolysis of P and release of hormones wouldbe a direct mechanism of mineralization of organic P (Joner et al.,2000; Tarafdar and Marschener, 1994) and process of chelation(Sharma and Sharma, 2013) enhanced rhizospheric P with VAMinoculation. It clearly proved that P was significantly solubilized byPSB and VAM in the rhizosphere.

Inoculation of PSB reduced the soil pH in both soybean andwheat crops during flower initiation stage (Table 4). PSB has beenreported to excrete a number of organic acids including lactic,glycolic, citric, gluconic, 2-ketogluconic, malic, oxalic, malonic,tartaric and succinic acids for solubilizing fixed P (Banik and Dey,1982; Mahanta and Rai, 2008). As acids, they have the effect ofdecreasing medium pH (Khan and Bhatnagar, 1977). Hence, thetreatments consisting inoculation of PSB have lower pH, closer tothe optimum P availability. As the levels of P (without PSB)decreased for soybean crop, the soil pH also decreased and thelowest value was recorded under control plots (7.23). Under Pdeficiency, legumes including soybean is known to extrude largequantities of organic acids, especially citric, malonic, malic and





succinic acids through roots (Mahanta and Rai, 2008) andsignificantly decrease the rhizosphere pH. The process is respon-sible for H+ extrusion under P stress, possibly through thedevelopment of rhizodermal transfer cells and increased activityof a membrane-located ATPase proton pump (Tang et al., 1998).This is the reason of lower pH, where P was not applied.

5. Conclusion

The results obtained from the experiment provide us withmajor findings about the influence of P and biofertilizers ondifferent root properties of soybean and wheat. Inoculation of bothPSB and VAM with 0.5 P increased P inflow rate by about 9.2 and4.6% in soybean and wheat, respectively, over 1.0 P treated plots.Increased root CEC and RLD might have been the cause of bettervalues of IPR, root and shoot P concentration and content in 0.5P + PSB + VAM plots compared to 1.0 P plots during flower initiationstage of soybean and wheat crops. The results of this study indicatethat 50% of recommended P application can be substituted byinoculation of both PSB and VAM for improved root properties andhigher productivity of soybean-wheat cropping system in Incepti-sol of semi-arid India.

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Influence of phosphorus and biofertilizers on soybean and wheat root growth and properties

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