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The intercropping cowpea-maize improves soil phosphorusavailability and maize yields in an alkaline soil
M. Latati & D. Blavet & N. Alkama & H. Laoufi &J. J. Drevon & F. Gérard & M. Pansu & S. M. Ounane
Received: 27 December 2013 /Accepted: 22 July 2014 /Published online: 10 August 2014# Springer International Publishing Switzerland 2014
AbstractAim This study assessed whether growing cowpea canincrease phosphorus (P) availability in the rhizosphereand improve the yield of legume-cereal systems. Inalkaline Mediterranean soils with P deficiency, it isassumed that legumes increase inorganic P availability.Methods A field experiment was conducted at theStaoueli experimental station, in Algiers province,Algeria, to compare the growth, grain yield, P availabil-ity, and P uptake by plants with sole-cropped cowpea(Vigna unguiculata L. cv. Moh Ouali) and maize (Zea
mays L. cv. ILT), intercropped cowpea-maize, andfallow.Results P availability in the rhizosphere was increasedin both sole cropping and intercropping systems com-pared with fallow. It was highest in intercropping. Theincrease in P availability was associated with (i) signif-icant pH changes of the rhizosphere of cowpea in solecropping and intercropping systems, with the rhizo-sphere acidification significantly higher in intercropping(−0.73 units) than in sole cropping (−0.42 units); (ii)significant increase in the rhizosphere pH of
Plant Soil (2014) 385:181–191DOI 10.1007/s11104-014-2214-6
Responsible Editor: Martin Weih..
M. Latati (*) : S. M. OunaneDépartement de phytotechnie, Ecole Nationale SupérieureAgronomique, Hassan Badi, El Harrach, Algiers, Algeriae-mail: [email protected]
S. M. Ounanee-mail: [email protected]
D. Blavet :M. PansuUMR Eco&Sols, IRD, 1 place Pierre Viala,34060 Montpellier, France
D. Blavete-mail: [email protected]
M. Pansue-mail: [email protected]
N. AlkamaFaculté des Sciences Biologiques et des SciencesAgronomiques, Département des Sciences Agronomiques,Université de Mouloud Mammeri, TiziOuzou, Algeriae-mail: [email protected]
M. Latati :H. LaoufiDépartement agronomie, Université de Bachir El Ibrahimi,Bordj Bou Arérridj, Algeria
H. Laoufie-mail: [email protected]
M. Latati : J. J. Drevon : F. GérardUMR Eco&Sols, INRA, 1 place Pierre Viala,34060 Montpellier, France
J. J. Drevone-mail: [email protected]
F. Gérarde-mail: [email protected]
M. LatatiRue de la revolution, collo, Skikda, Algeria
intercropped maize (+0.49 units) compared to fallow;(iii) increased soil respiration (C-CO2 from microbialand root activity) in intercropping compared with solecropping and fallow; and (iv) higher efficiency in utili-zation of the rhizobial symbiosis in intercropping than insole-cropped cowpea.Conclusion With cowpea-maize intercropping, cow-pea increased the P uptake, by increasing the P avail-ability by rhizosphere pH changes in an alkaline soil.Overall, this study showed that intercropping cowpeaimproved the plant biomass and grain yield of maizein this soil.
Keywords Pavailability . Intercropping .BiologicalN2-fixation . Rhizosphere acidification
Introduction
Fallow-cereal rotation is the usual cropping system forcereal production in Algeria. It is used extensively,covering more than 40 % of arable land, but contrib-utes only 50 % of the population’s cereal require-ments. With rising food prices, replacing fallow bylegume crops in the Algerian farming system hasbecome a strategic necessity for food security(Alkama et al. 2009).
Legumes can mitigate soil nitrogen (N) deficiencythrough symbiotic biological N2 fixation and phospho-rus (P) deficiency by changing the soil pH of the rootzone (Giller et al. 1997; Alkama et al. 2009;Betencourt et al. 2012). P deficiency is a major factorlimiting nodule formation and legume growth in manysoils, especially in Mediterranean and tropical zones(e.g., Alkama et al. 2009). The input of P via mineralfertilizers has been practiced for many years to im-prove legume yield (Dawson and Hilton 2011) but inthe future, availability of P fertilizers may becomeincreasingly limited by decreasing mineral P reservesand increasing food needs over the next 40 years(Dyson 1999). Another approach is to increase theavailability of P in soils, which is frequently limitedby its precipitation with cations such as Ca2+, Al3+, andFe3+ and its adsorption onto mineral particles(Hinsinger 2001). In this context, alternative agronom-ic practices and/or selection of plants and microorgan-isms that can use P efficiently are needed to solubilizesoil P in agroecosystems (Lambers et al. 2006; Zingoreet al. 2008).
Recent research has shown that the association ofcereals and legumes can increase yields and improveN and P uptake via the biological fixation of N2 andchemical changes within the root zone (Betencourt et al.2012; Latati et al. 2013), e.g., faba bean/maizeintercropping (Li et al. 2005). Mechanisms that help toalter the rhizosphere processes of both species have beendescribed (Zhang and Li 2003; Li et al. 2005;Betencourt et al. 2012; Latati et al. 2013), includingmechanisms affecting P availability especially in P-deficient soils (e.g., Li et al. 2007; Hinsinger et al.2011; Betencourt et al. 2012). Cereal-legumeintercropping can encourage rhizosphere acidificationthrough proton release by roots of N2-fixing legumes(Li et al. 2008). Conversely, alkalization can also in-crease rhizosphere P availability in noncalcareous soils(Hinsinger et al. 2003; Devau et al. 2011a). In a P-deficient soil, intercropping durum wheat and chickpeaincreased P availability in the rhizosphere of both spe-cies, although no acidification was found probably be-cause of the low rate of N2 fixation by chickpea(Betencourt et al. 2012). Carbon dioxide (CO2) emis-sions from the soil surface were also measured as anindicator of the overall activity of soil microorganismsand root-nodule symbiosis, as several components ofthis activity may be involved in the control of Pavailability.
This study considered four questions: (i) Does grow-ing cowpea as a sole crop or intercropped with maize inalkaline soils increase P bioavailability and P concen-tration in plants for both crops? (ii) Is there a measur-able pH change at the root zone related to the high rateof N2 fixation by cowpea? (iii) Does intercroppingcowpea and maize increase the growth and yield ofboth crops? (iv) Is there a difference in the formationand activity of symbiotic nodules on cowpea rootsbetween legume sole cropping and cereal-legumeintercropping?
Materials and methods
Experimental site
The field experiments were conducted during the 2013growing season at the Technical Institute of MarketGardening and Industrial Crops (Institut Technique desCultures Maraîchères et Industrielles, ITCMI). Thefarm is located in the Staoueli region, 20 km northwest
182 Plant Soil (2014) 385:181–191
of Algiers (36° 45′ 24″ N, 2° 53′ 8″ E). The annualrainfall is nearly 700 mm and the annual meantemperature is 17.9 °C. The soil of the experimentalsite was characterized by standard sampling ofthe top layer (0–30 cm) when the crops were sown.The soil is a Fersialsol containing approximately79 % sand, 11 % loam, and 10 % clay. The topsoilwas alkaline (pH 8.1), with 1.5 % CaCO3, 1.4 gtotal N kg−1, and was poor in organic matter(1.6 %). The P content corresponded to the agro-nomic conditions of P deficiency for most crops(Olsen-P=8.7 mg P kg−1).
Cropping system
The study was carried out with one cowpea cultivar(Vigna unguiculata L. cv. Moh Ouali) and one maizecultivar (Zea mays L. cv. ILT) commonly grown inthe Algerian cereal-legume agroecosystem. The ex-perimental design was a plot divided into fourblocks (four replicates), each block being furtherdivided into four plots. Each plot was used for oneof the following four cropping systems: cowpea,maize, maize intercropped with cowpea, and fallow.The experiment covered an area of 765 m2, eachplot being 15 m×3 m. Maize and cowpea wereplanted alternately in the same row with 25 cmbetween maize plants and cowpea plants. The plantdensity corresponded to current farming practice: 24±5 plants per m−2 for cowpea sole cropping, 15±3plants per m−2 for maize sole cropping, and 12±3plants per m−2 for each species in intercropping. Thesoil in the fallow plot was ploughed and leftunplanted according to local farming practices. Theseeds were sown on May 10, 2013. The crops weresown and cultivated by farmers using their normalpractices without any fertilization. The crops wereharvested at maturity: cowpea on August 25 andmaize on September 10.
Plant and soil samples
The first set of samples was taken 70 days aftersowing (DAS), which coincided with the fullflowering stage for both maize and cowpea. Theshoots were separated from the roots at the cotyle-donary node, dried for 48 h at 60 °C, and thenweighed. The nodules were separated from the roots,counted, dried, and weighed separately. Samples of
the soil from the fallow were taken as a control aswell as from the rhizosphere of each species(Hinsinger 2001) by brushing off the <1–4-mm ag-gregates of soil adhering to roots gently using apaintbrush. The rhizosphere of all plants sampled ofeach species was bulked for each replicate for eachcropping system. The rhizosphere samples were thenstored at 4 °C for no more than 3 days beforeanalysis.
The second set of samples was taken at harvest whenthe crops were mature. The crop yield was determinedby harvesting all the plants within 1 m2 blocks with fivereplicates in each plot, excluding the outer rows. The dryweight yields of both species were calculated after dry-ing for 48 h at 60 °C to give a water content in the rangeof 10–15 %.
For both sets of samples, the N concentration in therhizosphere soil was determined using the Kjeldahlmethod and the total P concentration in the plants(shoots, roots and grain) and soil was determined usingthe malachite green method after digestion by nitric andperchloric acid (Valizadeh et al. 2003). The soil P avail-ability was determined by NaHCO3 extraction (Olsenmethod), and the rhizosphere pH was measured in soilsuspended in purified water with a soil to water ratio of1:2.5 (Shen et al. 1996).
CO2 emissions
The CO2 emissions from the soil surface were alsomeasured as an indicator of the overall activity of thesoil microorganisms and root-nodule symbionts, giventhat several components of this activity may be involvedin controlling P availability.
To evaluate the cumulative microbial and root respi-ration in intercropping, sole cropping, and fallow, theCO2-C fluxes from the soil were measured at threestages of growth: 30 days after sowing (DAS), begin-ning of flowering (50 DAS), and full flowering(70 DAS). Field measurements were taken on fivereplicates per plot by titrimetry after CO2 absorptionfor 1 day in 20 mL of NaOH solution inside PVCcylinders (15.2-cm internal diameter and 27.5-cmlength) hermetically sealed on the sides and top andburied at a depth of 10 cm below the soil surface(Fig. 1). The respired CO2-C was estimated by precip-itating the carbonates with a solution of BaCl2 and bytitrating the remaining NaOH with a standard aqueoussolution at 0.25 mol HCl L−1. A fully sealed cylinder at
Plant Soil (2014) 385:181–191 183
the same temperature and humidity was used as acontrol. The CO2-C fluxes in grams per square meter
per day were calculated using the following equation(e.g., Chevallier et al. 1998):
gCO2−C m−2 d−1 ¼ 1=2 � 12xCHCI �ΔVHCI � 10; 000=Sð Þ 24=tð Þ = 1; 000
whereCHCl is the HCl concentration (mol L−1),ΔVHCI is the difference in the added volumes of HCl
solution between the control and the sample (mL),S is the surface area of the cylinder (cm2), andt is the duration of CO2 emission (h).
Statistical analysis
One-way analyses of variance (ANOVA) with thecropping system as a factor at a probability of 0.05 wereconducted on the plant and nodule biomasses; P con-centration in roots, shoots, and grain; pH and P Olsen inthe rhizosphere; and grain yield. Significant differencesbetween mean values were determined by Tukey’s mul-tiple comparison tests at a probability of 0.05. Therelationships between the shoot dry weight, nodule dryweight, and nodule count were tested by regressionanalysis. The statistical analyses were carried out usingStatistica eight.
Results
Plant growth, yield, and P allocation
The cowpea shoot and root biomass per plant decreasedsignificantly under intercropping by 48 and 31 %, re-spectively (Fig. 2).
The maize shoot biomass per plant increased signif-icantly (68%) under intercropping whereas there was nosignificant change for root biomass. The maize grainyield increased significantly by 25 % underintercropping compared to sole cropping, whereas thecowpea grain yield decreased by 58 % (Fig. 3).
The mean P concentration in shoots, roots, and grain(Fig. 4) increased in maize shoots and seeds (73 and18 %, respectively) under intercropping, whereas nosignificant difference was found in roots. By contrast,the P concentration in cowpea shoots, roots, and seeddecreased significantly under intercropping, by 16, 28,and 34 %, respectively (Fig. 4).
Nodule growth and shoot to nodule ratio
Figure 5 shows that the nodule count and biomass wereaffected significantly by intercropping compared to solecropping. When cowpea was intercropped with maize,the nodule biomass per plant decreased by 56 % and thenodule count increased by 26 % compared to cowpeagrown as a sole crop.
The efficiency in utilization of the rhizobial symbio-sis (EURS) defines a relationship between plant biomassand nodule biomass (Drevon et al. 2011). For eachcowpea plant, the shoot biomass was plotted againstthe nodule biomass (Fig. 6a), the slope of the linearregressions between nodule dry weight (NDW) andshoot dry weight (SDW) being a standard method of
Fig. 1 Cross section of a cylinderfor CO2 measurement (Chevallieret al. 1998)
184 Plant Soil (2014) 385:181–191
estimating the EURS. The EURS of cowpea inintercropping (143 g DW shoot g−1 DW nodule, r2=0.86) was higher than in cowpea as a sole crop(98 g DW shoot g−1 DW nodule, r2 = 0.44).Surprisingly, Fig. 6b shows a negative correlation be-tween the number of nodules (NN) and the NDW perplant when cowpea was intercropped with maize
(slope=−426.4, r2=0.67, p<0.05) and when it wasgrown as a sole crop (slope=−194, r2=0.38).
Rhizosphere P availability and pH
The Olsen P concentration in the rhizosphere was al-ways significantly higher in the cultivated plots than in
Fig. 2 Dry weight of shoots (a, b) and roots (c, d) for maize and cowpea in sole cropping and intercropping. Values are the mean of tenreplicates. Bars indicate standard errors. For each crop, letters show significant differences between cropping systems (P<0.05)
Fig. 3 Grain yields (Mg ha−1) of cowpea (a) and maize (b) in different cropping systems. Values are the mean of five replicates. Barsindicate standard errors. For each crop, letters show significant differences between cropping systems (p<0.05)
Plant Soil (2014) 385:181–191 185
the fallow. For cowpea compared with fallow (Fig. 7 a),the increase in P Olsen in the rhizosphere was higher inthe intercropping (62 % higher than in the fallow) thanin sole cropping (23 % higher than in the fallow). Formaize compared with fallow, the increase in Olsen P in
the rhizosphere was also higher in intercropping (24 %higher than in the fallow) than in sole cropping (only8 % higher than in the fallow) (Fig. 7c).
The results indicate significant acidification of therhizosphere pH of cowpea in sole cropping and
Fig. 4 Phosphorus (P) concentration in shoots (a), roots (b), andgrain (c) for cowpea and maize in different cropping systems.Values are the mean of four replicates. Bars indicate standard
errors. For each crop, letters show significant differences betweencropping systems (P<0.05)
Fig. 5 Dry weight of nodules (a) and number of nodules (b) for cowpea in sole cropping and intercropping. Values are the mean of tenreplicates. Bars indicate standard errors. For each crop, letters show significant differences between cropping systems (P<0.05)
186 Plant Soil (2014) 385:181–191
intercropping (Fig. 7 b). The rhizosphere acidificationwas significantly higher in intercropping (pH 0.73 lowerthan in the fallow) than in sole cropping (pH 0.42 lower
than in the fallow). For maize (Fig. 7d), however, therhizosphere pH increased significantly when maize wasgrown in association with cowpea (pH 0.49 higher than
Fig. 6 a Effect of intercropping on efficiency in utilization of therhizobia symbiosis (EURS) shown as the regression of shoot dryweight to nodule dry weight (see Fig. 4a). b Regression between
nodule dry weight and number of nodules in sole cropping andintercropping for cowpea (see Fig. 4b). Values are the means of tenreplicates harvested at full flowering
Fig. 7 Olsen phosphorus (a, c) and pH (b, d) in the rhizosphere ofcowpea and maize as sole crop and intercrop and in the fallow.Values correspond to the mean calculated with five replicates.Bars
indicate standard errors. For each crop, letters show significantdifferences between cropping systems (P<0.05)
Plant Soil (2014) 385:181–191 187
in the fallow) but there was no significant change in pHin maize grown as a sole crop.
Soil respiration
Figure 8 shows the field CO2 flux from soil includingmicrobial and root respiration in sole cropping and inintercropping. The C-CO2 flux depended significantly onthe cropping system. Figure 8 shows an increase in the C-CO2 flux between 30 and 50 DAS for all the croppingsystems, whereas the C-CO2 flux in the fallow wasstable. At 50 DAS, there was a considerable differencein the C-CO2 flux between intercropping (33 % higherthan the fallow) and both maize and cowpea when grownas sole crops (5 and 19 %, respectively, higher than thefallow). At the full flowering stage, the C-CO2 flux in thefallow increased almost reaching the same C-CO2 fluxlevel from cowpea and maize grown as sole crops. Theflux increased significantly in the intercrop and remainedsignificantly higher than in the fallow (+59 %).
Discussion
The major finding in this work is that cowpeaintercropped with maize considerably increased
rhizospheric P availability (see Fig. 7a–c) and P concen-tration in plants in both species (Fig. 4a–c). Most studiesreported depletion of P availability in the rhizospherevia plant root uptake during the crop cycle (Hinsinger2001; Hinsinger et al. 2011; Pan et al. 2008). Only a fewrecent studies have shown an increase in P availability inthe rhizosphere of durum wheat and chickpea (Devauet al. 2010, 2011b; Betencourt et al. 2012). However,these studies were conducted under controlled condi-tions using rhizobox and pot experiments.
The increase in P availability in the rhizosphere ofintercropped maize can be explained by acidificationof the legume rhizosphere (Betencourt et al. 2012). InP-deficient soils, rhizosphere acidification could con-tribute to the increase in P availability for legumessuch as common bean (Alkama et al. 2009, 2012). Theacidification of the cowpea rhizosphere may be relatedto a higher uptake of cations than anions (Tang et al.2004; Hinsinger et al. 2003; Alkama et al. 2009).Legumes relying on N2 fixation generally take upmore cations than anions and thus extrude proportion-ally more H+ than OH− in the root-soil interface tocompensate for positive electrical charges and regula-tion of pH in plant cells (Tang et al. 1997).Nevertheless, acidification of the cowpea rhizospherecould be directly related to an imbalance in H+
Fig. 8 Soil and root respiration (g C-CO2m2 day−1) for all cropping systems as a function of time. Values are the mean of five replicates.
Bars indicate standard errors
188 Plant Soil (2014) 385:181–191
production with the O2 consumed by nodules for N2
fixation (Alkama et al. 2012). These authors observeda correlation between H+ release and nodule perme-ability and suggested that part of the H+ release wasrelated to symbiotic N2 fixation. The nodule perme-ability controls the nodule respiration that suppliesATP for N2 reduction catalyzed by the bacteroidalnitrogenase within the infected zone of the nodules(Kouas et al. 2008).
Rhizosphere alkalization for intercropped maize maybe explained by positive interaction between pH and Ca.Such alkalization in the rhizosphere of maize (seeFig. 7d) agrees with previous studies on other cerealsintercropped with legumes (Zhang et al. 2004; Devauet al. 2011b; Betencourt et al. 2012). For maizeintercropped with legumes, this would lead to rhizo-sphere alkalization if Ca were not taken up by maize.These results are in agreement with Betencourt et al.(2012). However, the reduction in pH induced by cow-pea roots may help to increase the Ca availability as aconsequence of carboxylate solubilization. In contrastwith maize, the preferential uptake of Ca by cowpea,either in intercropping or sole cropping, may contributeto rhizosphere acidification. This hypothesis was con-firmed for the chickpea-wheat intercropping system inthe study by White and Broadley (2003).
For intercropped maize, the increase in P concentra-tion and plant biomass, associated with an increase ingrain yield (Fig. 4), is assumed to result from the posi-tive effect of cowpea on P availability. Li et al. (2004)reported an improvement in the growth of intercroppedmaize by improved P nutrition. For intercropped chick-pea, for which no facilitation was observed, these au-thors suggest that phosphatase activity produced bychickpea increased the mineralization of organic P andits absorption by the associated maize. Thus, the in-crease in grain yield for intercropped maize (Fig. 3b)may be a consequence of the observed increase in boththe P uptake and the plant biomass by increased Pavailability in the rhizosphere. The increase in cerealgrain yield by intercropping with a legume was reportedfor maize (Li et al. 2005; Dahmardeh et al. 2010) anddurum wheat (Zhang and Li 2003) intercropped withcowpea and faba bean, respectively. Legumes,intercropped with cereals, provide P and increase itsavailability for the intercropped cereals (Dahmardehet al. 2010; Betencourt et al. 2012).
For cowpea, more significant and more negative cor-relation betweenNN andNDWin intercropping (Fig. 6b)
may be due to competition between cowpea and maizethat reduces the rhizobial infection and increases theindividual nodule mass in compensation. Only a fewrecent studies have reported the effect of intercroppingon nodule growth (Betencourt et al. 2012; Latati et al.2013). Alternatively, the decrease in nodule biomass maybe caused by P deficiency in the soil and compensated byan increase in the number of nodules. The latter mighteven be due to a change in the population of rhizobiainvolved in the nodulation (Depret and Laguerre 2008)that might lead to an increase in N2 fixation by the givenmass of nodules under intercropping.
The field measurements of C-CO2 (Fig. 8) are in linewith those of Ibrahim et al. (2013), which showed agreater root-respiration for wheat than for faba bean inintercropping, with a simultaneous increase in root mor-tality of faba bean leading to an increase in microbialrespiration. In this study, the high root respiration inintercropping (Fig. 8) may also be due to the high rateof N2 fixation of cowpea that is strongly linked to bothrhizobia symbiotic activity as regulated by nodule per-meability to O2 diffusion (Schulze and Drevon 2005)and to other mechanisms controlling root and microbialrespiration. Nodules on legume roots increase the releaseof H+ through nodule respiration linked to N2 fixation(Tang et al. 1997; Hinsinger et al. 2003; Alkama et al.2009). The higher C-CO2 observed in the rhizosphere ofcowpea grown as a sole crop (Fig. 8) than inintercropping is consistent with the higher nodule bio-mass of cowpea grown as a sole crop. In our experiment,measuring the C-CO2 in the rhizosphere is considered aninitial approach to distinguishing root-induced processeswhich help to change P availability under P limitation inthe soil. CO2 emissions from the soil surface are theresult of the overall activity of soil microorganisms androot-nodule symbionts, given that several componentsof this activity may be involved in the control of Pavailability. Further research is required on a gradientfrom P deficiency to P sufficiency. Understanding otherfactors affecting P availability in the rhizosphere is re-quired to develop strategies for improving the symbioticrhizobial efficiency for intercropped legumes understressful conditions such as P deficiency.
Conclusion
This approach was based on changes in the rhizosphereof two species in an alkaline soil and on corresponding
Plant Soil (2014) 385:181–191 189
changes in P availability and P measured in the plants.The results showed that P availability increased signif-icantly in the rhizosphere of both maize and cowpeathan in the fallow but that this increase was greater inintercropping. The increase in P availability was associ-ated with (i) acidification in the rhizosphere of cowpeain intercropping or sole cropping, (ii) differentalkalization in the rhizosphere of maize, although thiswas significant only for intercropped maize, and (iii)increased root respiration in intercropping compared tosole cropping. The results suggest that P availability inthe rhizosphere is affected not only by pH changes butalso by the interaction with other root-induced processessuch as an increase in efficiency in utilization of therhizobial symbiosis and C-CO2 flux from microbial androot activity. However, species interactions resulted inan increase in growth only for maize in the alkaline lowP soil. There are many complex interactions, both pos-itive and negative, and the mechanisms increasing Pavailability were not sufficient to increase cowpeagrowth when intercropped with maize. Based on thestress-gradient hypothesis, the results suggest that bio-mass, grain yield, and P uptake facilitation would begreater in intercropping, in P-deficient soils.
Acknowledgments This work was supported by the Great Fed-erative Project FABATROPIMED of Agropolis Foundation,Montpellier, France, under the reference ID 1001–009 and thejoint project AUF-PCSI 59113PS012 and the laboratory of(ENSA) d’Algerie in cooperation with “Institut Technique desCultures Maraîchères et Industrielles” (ITCMI) in the Staouliregion. We would like to thank the “Laboratoire des resourcesphytogénétiques et des biotechnologies végétales” of ENSA forproviding the maize cultivar (ILT).
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