MINI-REVIEW

Soil microbes and plant fertilization

Mohammad Miransari

Received: 13 May 2011 /Revised: 8 July 2011 /Accepted: 28 July 2011 /Published online: 12 October 2011# Springer-Verlag 2011

Abstract With respect to the adverse effects of chemicalfertilization on the environment and their related expenses,especially when overused, alternative methods of fertiliza-tion have been suggested and tested. For example, thecombined use of chemical fertilization with organicfertilization and/or biological fertilization is among suchmethods. It has been indicated that the use of organicfertilization with chemical fertilization is a suitable methodof providing crop plants with adequate amount of nutrients,while environmentally and economically appropriate. Inthis article, the importance of soil microbes to theecosystem is reviewed, with particular emphasis on therole of plant growth-promoting rhizobacteria, arbuscularmycorrhizal fungi, and endophytic bacteria in providingnecessary nutrients for plant growth and yield production.Such microbes are beneficial to plant growth throughcolonizing plant roots and inducing mechanisms by whichplant growth increases. Although there has been extensiveresearch work regarding the use of microbes as a method offertilizing plants, it is yet a question how the efficiency ofsuch microbial fertilization to the plant can be determinedand increased. In other words, how the right combination ofchemical and biological fertilization can be determined. Inthis article, the most recent advances regarding the effectsof microbial fertilization on plant growth and yieldproduction in their combined use with chemical fertilizationare reviewed. There are also some details related to themolecular mechanisms affecting the microbial performanceand how the use of biological techniques may affect theefficiency of biological fertilization.

Keywords Arbuscular mycorrhizal (AM) fungi . Biologicalfertilization . Endopytic bacteria . Plant growth-promotingrhizobateria (PGPR)

Introduction

Plant growth and yield production are affected by differentparameters including soil, plant, and climate properties.Altering soil properties including physical, chemical, andbiological ones can influence plant growth and yieldproduction. There are different methods of adjusting soilproperties, resulting in enhanced soil production. For exam-ple, the addition of soil organic matter is a favorable way ofimproving soil properties (Böhme and Böhme 2006) byproviding a favorable soil structure, enhancing soil cationexchange capacity, increasing the quantity and availability ofplant nutrients, and providing the substrate for microbialactivities. However, the availability of plant nutrients is adetermining factor for plant growth and yield production.

Plants require macro- and micronutrients for theiroptimal growth and production. Among the differentmethods of enhancing nutrient quantity and availabilityfor plant utilization is the use of chemical fertilization,which is a fast way of providing plant with necessarymacro- and micronutrients. With the rapid growth ofworld population, the use of chemical fertilization hastremendously increased and hence the probability ofenvironmental pollution. The unfavorable effects offertilization overuse include leaching, runoff, emission,and eutrification of aquatic ecosystems (Flessa et al.2002; Vessey 2003; Ma et al. 2007; Adesemoye andKloepper 2009a; Adesemoye et al. 2009b; Yang et al.2009). Hence, it is important to optimize the use ofchemical fertilization to fulfill crop nutrient requirementsand to minimize the risk of environmental pollution.

M. Miransari (*)Department of Soil Science, College of Agricultural Sciences,Shahed University,Tehran 18151/159, Irane-mail: Miransari1@google.com

Appl Microbiol Biotechnol (2011) 92:875–885DOI 10.1007/s00253-011-3521-y

With respect to the effects of different parametersaffecting nutrient amount and availability, it is likely topredict the optimal amounts of nutrients for yield produc-tion (Miransari and Mackenzie 2010, 2011a, b). Nutrientavailability is a function of nutrient chemical properties,soil and climate properties, and plant species. Somenutrients like nitrogen (N) and potassium (K) have highermobility relative to the others such as phosphorous (P),calcium (Ca), magnesium (Mg), and micronutrients. Such aproperty can definitely influence nutrient availability andhence plant growth and yield production. Although thehigher mobility and availability of nutrients in soil makethem more available to crop plants, such a property can alsomake them more vulnerable to leaching, especially inhumid areas. Nutrients with less solubility can precipitateimmediately after being incorporated into the soil. Forexample, due to the little availability of P compounds, afterfertilizing soil with P products in the first year on average,only 20% of the P will be available to the plant and theremaining part would get precipitated (Miransari 2011a).

Furthermore, the environmental issues regarding the useof chemical fertilization is also of great significance asexcess amount of chemical fertilization results in thepollution of the environment. Chemical fertilization canalso influence the enzyme activities of soil microbes, soilpH, and soil structure (Böhme and Böhme 2006). It istherefore pertinent to apply the optimum amounts offertilization in the field. Accordingly, it can be favorablethat other methods of fertilization be also tested and used toprovide necessary nutrients for plant growth and yieldproduction, while keeping the soil structure in good shapeand the environment clean.

The alternative methods of soil fertilization are organicfertilization, including the addition of manure and plantresidue, the use of legumes as green fertilization, and theuse of soil microbes. The advantages of adding plantresidues are improved soil structure, enhanced nutrientavailability, and great benefits for environment. However,relative to chemical fertilization (in kilograms per hectare)the efficiency of organic fertilization is less because muchhigher amounts of organic fertilization (in tons per hectare)is necessary to supply the adequate amounts of plantnutrients.

The other alternative method of providing nutrients forplant growth and yield production is the use of soilmicrobes, which have been proved to be very advantageous(Adesemoye et al. 2008; Adesemoye and Kloepper 2009a;Adesemoye et al. 2009b; Berg 2009). There are a widerange of microbes in the soil, which are able to act insymbiotic or non-symbiotic association with their host plant(Gray and Smith 2005). Soil microbes are a great andnecessary part of soil ecosystem and can handle thefollowing important functions in the soil (Emmerling et

al. 2002; Böhme and Böhme 2006; Daei et al. 2009; Jalili etal. 2009; Lugtenberg and Kamilova 2009; Abbas-Zadeh etal. 2010; Arzanesh et al. 2010): (1) recycling soil nutrientsavailable in organic form, (2) enhancing soil nutrientavailability and hence their uptake by plant, (3) improvingsoil structure by producing different biochemicals, (4)controlling the adverse effect of pathogens on plant growth(Haas and Défago 2005), (5) alleviating soil stresses onplant growth and yield production, (6) biofertilization, (7)enhancing root growth, and (8) rhizoremediation.

Plant growth-promoting rhizobateria (PGPR) are amongsuch soil microbes greatly contributing to enhanced plantgrowth and yield production. However, it is yet a questionthat how complementary can be the use of organic ormicrobial fertilization to chemical fertilization. In otherwords, how the efficiency of chemical fertilization can beincreased by using the alternative methods of fertilization,with respect to the environmental and economical points ofviews. There are also bacterial endophytes, which areassociated with plant tissues enhancing plant growth andyield production under different conditions including stress.The host plant is able to provide a suitable environment forthe bacteria in exchange for the benefits, which are suppliedby the host plant. For example, some endophytic bacteriaare diaztrophic and can fix N.

Plant growth-promoting rhizobacteria

Among the most effective soil bacteria, which can promoteplant growth, are PGPR. Such bacteria are able to colonizeroot surface, as a result of some signal communicationsbetween the host plant and the bacteria (Bianciotto et al.2000). PGPR include a wide range of soil microbesincluding the microbes, which are in symbiosis with theirhost plant-like rhizobioms, fixing atmospheric N2, and theones, which are not in symbiotic association with their hostplant such as Pseudomonas spp., Bacillus spp., Azospirilumspp., and Burkholderia spp. (Glick et al. 1998).

In their association with their host plant, PGPR maydifferently colonize their host plant. They may colonize therhizosphere, the root surface, or the intercellular spaces of thehost plant. The colonizing ability of PGPR is determined byutilizing organic acids rather than sugars, their chemotaxisresponse and mobility, and production of lypopolysaccharidesand proteins (Lugtenberg and Bloemberg 2004; Lugtenbergand Kamilova 2009).

The benefit of the host plant to PGPR includes theproduction of organic products by the plant roots(rhizodeposition), utilized by PGPR in the rhizosphere,on plant roots or the in the intercellular places callednodules (rhizobium). Nodules are the intimate structureof the differentiated root cells for the fixation of

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atmospheric N2 by rhizobium. Soil rhizobium in the generaRhizobium, Bradyrhizobium, Sinorhizobium, Azorhizobium,Mezorhizobium, and Allorhizobium belong to the familyRhizobiaceae and are collectively called rhizobia invadingthe host plant root and fixing atmospheric N2 (Martinez-Romero and Wang 2000).

Rhizosphere is the soil environment for root growthand is specified by the high volume of root productsand hence microbial population. Soil microbes areusually distributed in a 50-μm distance from the plantroot and at the 10-μm distance their population mayincrease up to 109–1012/g soil. However, interestingly,although a large microbial population is present in therhizosphere only 7–15% of plant roots are colonized bysoil microbes (Pinton et al. 2001).

The signal communications between the bacteria and thehost plant are an important stage in the establishment ofsymbiosis between the host plant and the symbiotic bacteria(i.e., rhizobium) or the non-symbiotic bacteria, whichcolonize the plant roots. In such kind of communications,the plant and the bacterial genes are activated in somechemotactic responses to the production of biochemicalsubstances by the two sides. Ultimately, the formation ofroot nodules and the production of different substances bythe two symbionts are the results of such kind ofassociations (Miransari and Smith 2007; 2008; 2009).

Hence, it is important to identify microbial genes,which are responsible for plant growth promotion. Theexpression of such genes results in the production ofsubstances, which can enhance plant growth. Themicrobes can be accordingly handled and if necessarythe plant growth-promoting genes can be inserted inother microbes. For example, Choi et al. (2008)indicated that the production of a cofactor, pyrroloquino-line quinine (PQQ) by Pseudomonas fluorescence B16, isamong the important parameters conferring the ability ofplant growth promotion to the bacteria. They were able toidentify and isolate the responsible genes. PQQ can bedissolved in water, is resistant under heat stress, and canhandle redox reactions (Stites et al. 2000). PQQ has beenhighly researched because it is present in a wide range offoods and has antioxidant activities (Kumazawa et al.1995; He et al. 2003; Lugtenberg and Kamilova 2009).

As previously mentioned, different nutrients arenecessary for plant growth and yield production.Chemical fertilization is a fast way of providing plantswith their necessary nutrients. However, because of thefollowing deleterious effects on the environment, theymust not be used at high rates: (1) the increasedconcentrations of NO3, which is not recommendable atconcentrations higher than 50 mg/l, in different water sources(surface and ground) by WHO, (2) their unfavorable effectson the soil structure and soil pH, and (3) the emission of

greenhouse gases such as N2O. Accordingly, researchershave tested and proved the methods by which theefficiency of PGPR including rhizobium–plant symbiosiscan be enhanced under different conditions includingstress (Gray and Smith 2005).

Interactions between plant and endophytic bacteria

The endophytic bacteria, which are usually present in planttissues are able to enhance plant abilities and hence growth.Interestingly, numerous research works had indicated theapplications of natural and genetically modified endophyticbacteria for the alleviation of stresses. The endophyticbacteria can also significantly contribute to enhancing plantgrowth and hence can be assumed a source of fertilizationfor the host plant (Reinhold-Hurek and Hurek 1998;Kuklinsky-Sobral et al. 2004; Luo et al. 2011).

Luo et al. (2011) have indicated that the use ofendophytic bacteria is a useful phytoremediation methodunder heavy metal stress as the bacteria are able to absorbsignificant amounts of heavy metals. They isolated theendophytic bacteria LRE07 from the hyper accumulatorhost plant Sorghum nigrum. Using the 16S rRNA sequenceanalysis, the bacteria were identified as Serratia sp. withthe following abilities: (1) resistant under the stress ofheavy metals, (2) solubilization of mineral phosphate, and(3) production of auxin and siderophore (Sziderics et al.2007). In addition to the tolerance of the bacteria underheavy metal stress, the latter abilities can also significantlyenhance plant growth. Both under single- and multi-ionstress, the bacteria were able to bind significant amounts ofmetals in their cells. For example, 72 h after beingsubjected to the stress, the bacteria absorbed 65% ofcadmium and 35% of zinc.

In addition, there is also endophytic actinobacteria,which have been the center of attention by researchers indifferent disciplines. They are able to produce a widerange of secondary metabolites with biological propertiesincluding antimicrobial products, plant growth promoters,and enzymes resulting in the enhancement of plant growthunder different conditions including stress. They canaccordingly have pharmaceutical, industrial, agricultural,and hence biotechnological applications, although muchmore research must be performed in this regard (Qin et al.2011).

The use of recent metagenomic methods includinggenome scanning and sequencing has made possible theidentification of gene clusters, which can confer thebacteria such kind of abilities. The new methods can alsohelp identify the new bacterial products (for examplepharmaceuticals), which can be used for different usagessuch as therapeutic. The use of genome sequencing can

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more clearly clarify the mechanisms related to the inter-actions between the endophytic bacteria and the host plantand hence increase their biotechnological applications (Qinet al. 2011).

Effects of soil microbes on the soil ecosystem

Enhancing nutrient uptake

Soil microbes including arbuscular mycorrhizal (AM) fungiand PGPR are able to enhance the availability of differentnutrients by utilizing different mechanisms including theproduction of different enzymes. AM fungi can enhance thesolubility and availability of different nutrients including Pand micronutrients by producing phosphatases, which canenhance P availability to the plant under different con-ditions including soil stresses. AM hypha is able to grow inparts of the soil, which plant roots are not able to grow. It isbecause AM hypha is finer than even the finest plant roothairs and hence grows into the smallest soil microporesabsorbing water and nutrients. Such a character cansignificantly enhance plant roots absorbing surface andhence the uptake of water and nutrients (Hodge et al. 2001;Harrier 2001; Tanaka and Yano 2005; Miransari et al.2009a, b).

PGPR are also able to enhance the availability ofdifferent nutrients including N, P, and micronutrients. Forexample, Rhizobium spp., in symbiosis with their legumehost plant, and Azospirillum in non-symbiotic associationwith their host plant can fix atmospheric N2 (Miransari andSmith 2007; 2008; 2009; Abbas-Zadeh et al. 2010;Arzanesh et al. 2010). PGPR including Bacillus spp. P.fluorescence and Pseudomonas putida are able to enhanceP availability by production of organic acids and phospha-tase enzymes (Glick et al. 1998; Jalili et al. 2009; Abbas-Zadeh et al. 2010; Zabihi et al. 2010). Through producingsiderophores, PGPR can also increase Fe solubility andhence uptake by plant (Lugtenberg and Kamilova 2009).

Recycling organic nutrients

Some of the soil microbes are able to mineralize soilorganic matter in the soil. Although usually are notamong soil PGPR, however, their presence in the soil isvery important because they make nutrients available toplants and microbes by recycling them in the soil. Forexample, in areas with acceptable level of soil organicmatter, soil-nitrifying bacteria are able to mineralizeorganic N to nitrite and then to nitrate, which can beabsorbed by plants. The other nutrients in soil organicmatter can also become available to plants and microbesby soil microbes. It is because soil microbes have the

necessary enzymes for nutrients turnover. Soil microbescan act very specifically in that regard because theyhave some of enzymes for the mineralization of soilorganic matter (Böhme and Böhme 2006).

Soil organic matter is a more efficient and useful sourceof energy for soil microbes as determined by parametersincluding qCO2 (CO2–microbial C). Chemical fertilizationresults in higher qCO2 values indicating that under suchconditions soil microbes are more stressed relative to theuse of organic fertilization, or soil microbes must use higherrate of energy to compensate for the adverse effects ofstress. Soil fungi have a lower rate of qCO2 than soilbacteria, indicating that soil fungi are more efficient thansoil bacteria (Böhme and Böhme 2006).

Improving soil structure

Soil particles are bound by organic chemicals includingcompounds produced by soil microbes. A wide range ofbiochemicals are produced by soil microbes among whichpolysaccharides are the ones with the highest impact onbinding soil particles. In addition, AM fungi are able toproduce a glycoprotein called glomalin, binding soilaggregates, and hence improving soil structure. Similar toplant roots, AM hypha by itself can also bind soil particlesand hence results in the production of soil aggregates. Themineralizing effect of soil microbes on organic matter canalso influence soil structure. The enhanced growth of plantgrowth by soil microbes and hence the increased amount ofroot exudates and rhizodeposition can also affect soilstructure directly or by increasing the microbial populationand activities, indirectly (Rillig and Mummey 2006).

Controlling pathogens

Soil microbes produce a wide range of biochemicalsaffecting soil environment. Among which are the productsadversely affecting the growth and activities of soilpathogens including soil bacteria and soil fungi. Forexample, PGPR produce hydrogen cyanide (HCN), whichcan have unfavorable effects on the growth of soilpathogens. In addition, through stimulating plant systemicresistance, soil microbes can enhance plant resistance topathogens (Principe et al. 2007; Jalili et al. 2009). Thepresence of soil microbes in the rhizosphere and theproduction of different compounds can stimulate plantgrowth and systemic resistance. This is through theexpression of plant genes, which can in turn produce someproducts affecting plant resistance to pathogens or theproduction of root exudates, which can affect soil microbialpopulation and activities in the rhizosphere (Principe et al.2007). For example, Ryu et al. (2003) indicated that theinduction of systemic resistance (ISR) in plant is stimulated

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in the presence of Bacillus spp. through the production ofvolatiles including butanediol and acetoin.

Generally, the adverse effects of PGPR, which is mostlyrelated to Pseudomonas spp. and Bacillus spp. on soilpathogens is through the following: (1) production ofantibiotic compounds (HCN, pyrrolnitrin, phloroglucinols,phenazines, pyoluteorin, and cyclic lipopeptides), which forexample can inhibit electron transport (2) plant-inducedsystemic resistance, and (3) interfering with pathogensability to suppress plant growth, for example throughdegrading unfavorable products produced by the pathogen(Haas and Défago 2005; Qin et al. 2011). It has beenindicated that the pathway resulting in the production ofjasmonate/ethylene production is more important than thesalicylate-related pathway for plant ISR (Ton et al. 2002;Verhagen et al. 2003).

In addition, PGPR are able to alleviate the adverseeffects of stresses on plant growth through differentmechanisms. The alleviating effects of PGPR on plantgrowth enhances if the strains are isolated from the soilsunder stress. If the strains are isolated from soils, which aresubjected to salinity or acidity or drought they can moreeffectively alleviate the stress (Daei et al. 2009; Jalili et al.2009). Furthermore, there are also other mechanisms bywhich PGPR can enhance plant growth under stressincluding: (1) enhanced production of osmolytes underdrought or salinity stress, (2) enhanced activities of plantantioxidants, which can catabolize the stress products, (3)production of different metabolites by PGPR or by plant asa result of the symbiotic association, (4) production of 1-aminocyclopropane-1-carboxylate (ACC) deaminase,which can help plant survive under stress, (5) thesolubilization of insoluble P productions, (6) siderophoreproduction, (7) inhibition of pathogens (Chebotar et al.2009), and (8) adjustment of ions ratio for example K/Na+

under stress.

Alleviating soil stresses

In the recent years, there have been some very interestingresearch works regarding the use of PGPR under stress. Forexample, Glick et al. (1998) indicated that under differentstresses PGPR such as P. fluorescence and P. putida canalleviate the adverse effects of stress on plant growththrough the production of the bacterial enzyme ACCdeaminase. ACC is the prerequisite for the production ofethylene whose amounts are increased under stress ad-versely affecting plant growth and yield production. Hence,ethylene is one of the stress hormones regulating plantgrowth under different conditions including stress.

Production of ACC deaminase by PGPR can turn ACC,which is the prerequisite for ethylene production into NH3

and α-ketobutyrate and hence control the stress. ACC

deaminase is also able to increase root growth under stress,affecting plant growth. In addition, the alleviating effects ofAM fungi on plant growth under different stressesincluding salinity (Daei et al. 2009) and soil compaction(Miransari et al. 2007; 2008; 2009a, b) have been indicated.

There are also other soil stresses affecting plant growth andyield production including soil pH, suboptimal root zonetemperature, and heavy metals. Interestingly, researchers havefound that the adverse effects of different stresses on theRhizobium–legume N fixation can be alleviated by the use ofsignal molecule such as genestein. Geneistin is produced bythe specific legume host plant like soybean (Glycine max L.)activating the nod genes in Bradyrhizobium japonicum(Miransari and Smith 2007; 2008; 2009).

Under humid or dry climate conditions, soil pH canfluctuate very much. The high amount of rain in the humidarea reduces soil pH significantly through leaching alkalinecations such as Ca and Mg or enhancing the weatheringprocesses, which eventually result in the production of ironand aluminum oxides with a high affinity for the exchangeof protons with the soil solution. Under dry climateconditions, there is a high concentration of alkaline cationsin the soil including Ca and Mg, which considerablyincrease soil pH. Soil acidity can affect soil efficiencythorough affecting: (1) plant growth and yield production,(2) microbial population and activities, (3) soil nutrientavailability, and (4) pathogen activities.

Plants can grow and produce optimum yield underoptimal soil pH, however, deviations from favorable pHcan adversely affect plant growth and yield production. It isbecause different physiological mechanisms in the plant arecatalyzed by different enzymes, which can act at afavorable pH. Unfavorable pH can decrease plant growthby adversely influencing the enzyme activities in the plantand the cellular pH, whose optimum level is necessary forappropriate cell activities. Plants can adjust their cellularand rhizosphere pH by different mechanisms. For example,production of different biochemicals in the plant cells canadjust cellular pH, affecting microbial activities andnutrient solubility and hence availability.

A wide range of organic products are produced byplant roots by the process of rhizo-deposition includingcarbohydrates, organic, and carboxylic acids can significantlyinfluence plant rhizosphere including its microbes. Suchproducts are a significant carbon source and hence food forsoil microbes. They can affect microbial activities for exampleas signal molecules activating the microbial genes insymbiotic or non-symbiotic association with their host plant,adjust soil pH by producing H+ and hence the availability ofsoil nutrients (Benizri and Amiaud 2005). In addition,plant growth stage and root properties can influence therhizodeposition properties. There are different parametersaffecting the quantity and quality of rhizodeposition

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including temperature, light, CO2, and agricultural practi-ces (Rovira 1959; Cheng and Johnson 1998; Nicol et al.2003).

Rhizodeposition is used for the process of rhizoreme-diation. Usually, some of the inoculants, which are appliedinto the soil for the alleviation of stress may becomeinactive due to several reasons such as the competition withother soil microbes and soil properties. For example, in theprocess of pollutant degradation in soil, because thebacteria may not be able to use the pollutant as a sourceof energy, they may starve and hence become inactive. Dueto this, researchers have used the method of growingbacteria in the laboratory and hence inoculating in the soilnear to the roots. Hence, the bacteria will be able to use rootexudates as a source of energy and hence degrade thepollutants (Kuiper et al. 2001; 2004).

Furthermore, the genetic combination of soil microbes isinfluenced by agricultural practices. It is because agricul-tural practices and soil and climate properties influenceplant diversity and accordingly the quality of plantrhizodeposition and soil organic matter and hence thegenetic combination of soil microbes is affected (Quideauet al. 2001; Warembourg and Estelrich 2001).

Different soil microbes including AM fungi and PGPRare able to alleviate salinity stress on plant growth. AMfungi, as previously mentioned, can significantly increaseplant water and nutrient uptake through their extensivehyphal network. This can be very advantageous underdifferent conditions including salinity. AM fungi can alsoalleviate the salinity stress on plant growth and hence yieldproduction by adjusting the ratio of Na+ and Cl− in theplant. Mycorrhizal plants are able to absorb higher rate of Kunder salinity, adjusting the K/Na ratio in the plant andhence alleviating the stress (Daei et al. 2009). Under stress,plant allocates more C to their roots, which can bebeneficial to the plant under stress (Miransari and Smith2007; Miransari et al. 2007; 2008). In addition, AM fungican also intensify such a process by enhancing plant Puptake, which can significantly increase root and henceplant growth.

PGPR can also alleviate salinity stress on plant growth.They are able to produce the important bacterial enzymeACC deaminase under different conditions including stress,which can effectively control the stress. This is because, aspreviously mentioned, ACC deaminase can catalyze theACC, which is the prerequisite for the production of thestress hormone, ethylene. Increased level of ethylene in theplant can adversely affect plant growth and yield produc-tion (Glick et al. 1998; Jalili et al. 2009).

Plant physiological and morphological characters arealso very important in the alleviation of stress in symbioticor non-symbiotic association with their host plant. Themore resistant plant species can perform more efficiently

under stress and their symbiosis with their host plant alsocan enhance such abilities. However, selecting the rightcombination of AM species and host plant to achieve thehighest likely efficiency under stress is also important (Daeiet al. 2009). It has been indicated that some PGPR are ableto produce polysaccharide products, binding Na+ in the rootzone and hence alleviating the stress of salt on plant andmicrobial growth and activities (Han and Lee 2005).

PGPR can also enhance P solubility and hence availabilityby producing different enzymes including phosphatase andalso by increasing plant root growth. For example, this can beachieved by controlling the activities of stress hormones suchas ethylene or by altering plant root rhizodeposition. (Glick etal. 1998; Jalili et al. 2009; Abbas-Zadeh et al. 2010; Zabihi etal. 2010). Plants are able to produce extracellular phospha-tase, as the molecular pathways for the production ofphosphatase have been indicated (Miller et al. 2001; Georgeet al. 2008; Richardson et al. 2009). Plants use differentstrategies to improve their P uptake efficiency indicated inthe following.

(1) Adjustment of their root morphology, for example byproducing more lateral roots, which can be used for plantselection for breeding (Lynch 2005; Liao et al. 2008), (2)the ability of plant species for the production of organicacids; there are some plant species such as chick pea andpigeon pea, which are efficient in producing organic acids.This can be advantageous, especially under rotation,because cropping plants with higher efficiency to produceorganic acids prior to the less efficient plants can enhance Pavailability in the soil for a longer time for the followingcrop (Wouterlood et al. 2004a, b), (3) the altered expressionof genes, producing organic anions, can be effective inplants, with the low ability to produce organic onions. Forexample citrate synthase, which is the important enzyme forthe production of citrate, as well as phosphoenolpyruvatecarboxylase and malate dehydrogenase have been testedand shown to be promising in some cases. In addition, thealteration of other genes, including the ones responsible forthe production of citrate permeable and malate channels,transferring the anions from the roots to the rhizosphere canalso be used as the alternative (Sasaki et al. 2004), and (4)the ability of plants to produce phosphatase, which isanother approach for breeding selection (Richardson et al.2009).

The other important effect of PGPR on plant growth isthrough controlling soil pathogens. Lugtenberg and Kamilova(2009) have indicated the following important mechanismsby which the interaction between PGPR and the host plantcan control the stress of pathogens on plant growth. (1)Antagonism between PGPR and soil pathogens can alleviatethe stress of pathogen on plant growth, (2) signal interfer-ence, the communications of signals between PGPR and thehost plant may adversely affect the activity of pathogens,

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which may similarly respond to the presence of host theplant, (3) predating and parasitizing, by praying the pathogenor by parasite activities the microbe may control soilpathogens, although must be much more investigated, (4)ISR, the enhanced plant resistance by PGPR can adverselyaffect pathogen growth and activities, (5) competition fordifferent nutrients and niches including iron, and (6)interference with the growth and activities of soil pathogens.

Interaction between soil microbes

There is a wide range of microbes in the soil, whichcontribute to some of the most important processes in thesoil necessary for efficient soil production. In addition, soilmicrobes are interactive antagonistically or synergisticallyaffecting their efficiency in the soil. Such a property canalso influence the production and use of bioinoculants.Among the most influential interactions between differentsoil microbes are the interactions between arbuscularmycorrhizal fungi and soil bacteria (Artursson et al. 2006;Miransari 2011b).

AM fungi are able to alter soil bacterial combination byaffecting root growth and hence rhizodepositions, which areimportant sources of nutrients and secondary metabolitesfor soil bacteria in the mycorrhizosphere (Gryndler 2000;Miransari 2011b). In addition, through other effectsincluding: (1) the competition for nutrients and (2) thehighly specific responses of some bacteria to certain AMspecies, which is due to the production of some AM fungalproducts including polysaccharides (Artursson and Jansson2003; Toljander et al. 2006), the interactions between AMand soil bacteria can be very significant (Miransari 2011b).

Different researchers have indicated the positiveinteractions between AM fungi and PGPR includingPseudomonas spp., Bacillus spp., Paeinibacills spp.Rhizobium spp., and Entrobater spp. Gram-positivebacteria may be more associative with AM fungi relativeto Gram-negative bacteria. PGPR may also be able tocolonize AM hypha (Hildebrandt et al. 2002; Artursson etal. 2006: Miransari 2011b).

PGPR and fertilization

PGPR can be used for alleviating the unfavorable effects ofstress on plant growth singly or in combination with otherforms of fertilization including chemical and organic toincrease plant growth and yield production. The selectionof the appropriate strains for the enhanced efficiency ofPGPR under different conditions is of significance. Itindicates that PGPR must be exactly screened for theirgrowth-promoting characters and be tested under different

conditions including stress for the selection of the mostefficient strains.

As previously mentioned, different strains of PGPR canenhance the availability of different nutrients. Rhizobiumspp. and Azospirillum spp. can fix N and hence areimportant in combination with N fertilization. In otherwords, at the time of inoculating plants with Rhizobium or/and Azospirillum it must be exactly indicated that if thebacteria alone are able to supply the host plant withadequate amount of N. Otherwise, N fertilization must alsobe utilized to provide the plant with its N requirement.

Usually for legumes the rhizobium is able to fix N athigh amount so that additional fertilization would not benecessary, though N fertilizer may be used as starter.However, in the case of PGPR including Azospirillum,although atmospheric N is fixed by the bacteria, it is notadequate for the plant requirements. Hence, N chemicalfertilization would also be necessary to supply N foroptimal plant growth and yield production. For P there arealso some similarities, although the P-solubilizing microbesusually cannot provide the complete P requirement foroptimal plant growth (Zabihi et al. 2010).

Soil P-solubilizing microbes including AM fungi andbacteria can enhance P solubility by producing enzymessuch as phosphatase. The interesting point is that thesynergistic interactions between AM fungi and PGPRincluding N-fixing Rhizobium can enhance the efficiencyof soil microbes. Especially, in the tripartite symbiosis,AM hypha can result in the movement of soil bacteria insoil (Bonfante 2003; Artursson et al. 2006). This is ofgreat importance for the production of biofertilizersbecause the right combination of soil microbes canenhance the biofertilizer efficiency (Adesemoye et al.2008; Yang et al. 2009).

A very interesting and important point about thecombined use of soil microbes and chemical or/and organicfertilization is to determine their appropriate rates. This is ofenvironmental and economical significance. There areseveral important key issues about this: (1) the microbialpotential for providing nutrients under certain conditionsfor plant utilization, (2) plant species, (3) soil properties,and (4) climate properties.

Soil microbial potential for enhanced nutrient availabil-ity differs under different conditions. Such abilities must betested to determine the microbial capacity for providingnutrients for plant use. Plant species are also of greatimportance as there are high variations among differentplant species for their nutrient requirements. Soil propertiescan affect both plant and microbial growth. Climateproperties affect microbial activities and plant growth andhence the related fertilization rates.

According to Berg and Smalla (2008), a set of parametersincluding biotic (i.e., plant species), abiotic (i.e., soil types),

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rhizosphere competence (i.e., plant hormones), and positiveand negative interactions (i.e., pathogens) influences thecommunity of rhizosphere microbes. Such parameterscan importantly affect biofertilization. They have indi-cated that the effects of plant species and soil type onthe structure of microbial combination in the rhizo-sphere are of significance. Hence, for each plant speciesand soil type, the appropriate biofertilizer must beselected to have the optimum utilization for plantgrowth. The use of new molecular and biotechnologicaltechniques has made the advance of the field morerapid. Accordingly, it is possible to trace the behaviorof biofertilizer in soil and try methods or techniques,which may increase the efficiency of biofertilization.

The other important parameter, which may influence theefficiency and applicability of biofertilization, is climatechange effects. Compant et al. (2010) reviewed 135 studieson climatic parameters including elevated CO2, drought, andwarming. Accordingly, they indicated that while AM fungiare positively affected by elevated CO2, the response of soilmicrobial communities was very variable, although in mostcases it was positive. The performance of soil microbesunder varying temperature was very different; however,PGPR and AM fungi significantly enhanced plant growthunder drought stress. Such results are of practical importancein biofertilization. To use biofertilizer, it must be clearlyindicated that under certain climatic conditions the biofertil-izer may perform efficiently with respect to the microbialcombination in it. It must be mentioned that the adaptivemechanisms used by plant and microbes under differentclimates may also affect the efficiency of biofertilization.

For example, under humid conditions, mineral nutrientsin different form of fertilization are subjected to leaching,which can definitely affect the fertilization rates. It has beenindicated that with respect to the higher levels of soilorganic matter under humid conditions and the subsequentmineralized nutrients, such amount of nutrients must alsobe noticed when developing fertilization recommendations(Miransari and Mackenzie 2010, 2011a, b). This can havesimilarities to the combined use of soil microbes andchemical or/and organic fertilization.

PGPR efficiency to increase plant growth is dependent onthe level of nutrients in the soil. According to Carlier et al.(2008), Adesemoye et al. 2008; Adesemoye and Kloepper2009a, and Zabihi et al. (2010) an increased level of NPKfertilization decreased the efficiency of Pseudomonas spp.They attributed such observation to the production of stresslevel of ethylene under low levels of NPK, whoseprerequisite is catabolized by ACC deaminase to NH3 andα-ketobutyrate. In addition, root growth and efficiency are ofgreat importance under nutrient deficiency and higher rootgrowth results in higher nutrient uptake and hence plantgrowth. Accordingly, PGPR, with higher efficiency under

nutrient efficient conditions, are able to increase plant growthby enhancing root growth and hence nutrient uptake (Glicket al. 1998; Jalili et al. 2009; Zabihi et al. 2010).

Determining the efficiency of chemical and biologicalfertilization is of significance as the contribution and hencethe optimum rate of each would be clearly indicated. It hasbeen indicated that PGPR are not a complete replacementfor chemical fertilization with higher efficiency (Zabihi etal. 2010; Salimpour et al. 2010). For example, Canbolat etal. (2006) examined the effects of chemical and biologicalfertilization on plant growth and nutrient uptake andindicated that chemical fertilization resulted in higherNPK uptake by plants. However, on the other hand, Elcokaet al. (2008) indicated that the efficiency of biologicalfertilization is a matter of microbial combination as doubleand triple inoculation with PGPR may significantlyenhance the biofertilizer efficiency. Shaharoona et al.(2008) and Cruz et al. (2009) indicated that the perfor-mance of Pseudomonas spp. in enhancing plant growth isfertilizer dependent. However, more research is necessaryto clearly indicate the contributing role of chemical andbiological fertilization in providing necessary nutrients forplant growth and yield production.

According to the research, conducted so far, the use ofchemical fertilization is necessary as biological fertilizationhas not yet proven to be good enough for completelyproviding plant nutrient requirement. However, whatmatters about chemical fertilization is to enhance itsefficiency environmentally and economically using biofer-tilizers. It has been indicated that about less than 50% ofchemical fertilizers is absorbed by plant and the rest wouldnot be accessible by plant as it is subjected to leaching,runoff, and emission from the soil surface (Adesemoye etal. 2009b). Hence, the use of biological fertilizers assupplementary fertilization to chemical fertilization isnecessary with the abovementioned advantages. Accord-ingly, the right and proper application of chemical andbiological fertilization is very much dependent on realizingthe interactions between soil, plant, and microorganisms.Soil microbes are a big help to plant and the environment asthey own some great abilities that collectively enhanceplant growth. Among such abilities, enhanced nutrientuptake by plant is also of great importance; in the presenceof soil microbes, plant absorbs higher amounts of nutrientsand less risk of environmental pollution is likely.

Conclusion

Some of the most important functions of soil microbes werereviewed in this article. However, the particular emphasishas been on the use of soil microbes including AM fungi,Rhizobium, and other PGPR for biological fertilization.

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Chemical fertilization is a very common method ofproviding plants with their necessary nutrients because ofits rapid effects on plant growth and yield production.However, there are important issues regarding the use ofchemical fertilizers, as their improper and excess use canadversely affect the environment. Accordingly, it is impor-tant to indicate the contribution of chemical and biologicalfertilization to the plant growth. This can be used for thedevelopment of proper methods of fertilization. For theefficient development of biofertilizers, the microbes mustbe properly selected, combined, and formulated withrespect to the conditions. The appropriate use of fertiliza-tion, which is a combination of chemical and biologicalfertilization, can very much contribute to the enhanced foodproduction in the world, while economically and environ-mentally recommendable.

References

Abbas-Zadeh P, Saleh-Rastin N, Asadi-Rahmani H, Khavazi K,Soltani A, Shoary-Nejati AR, Miransari M (2010) Plant growthpromoting activities of fluorescent pseudomonads, isolated fromthe Iranian soils. Acta Physiol Plant 32:281–288

Adesemoye A, Kloepper J (2009) Plant–microbes interactions inenhanced fertilizer-use efficiency. Appl Microbiol Biotechnol85:1–12

Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plantnutrient use efficiency with PGPR and AMF in an integratednutrient management system. Can J Microbiol 54:876–886

Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates ofchemical fertilizers. Microbial Ecol 58:921–929

Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immuno-capture to identify active bacteria associated with arbuscularmycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215

Artursson V, Finlay R, Jansson J (2006) Interactions betweenarbuscular mycorrhizal fungi and bacteria and their potential forstimulating plant growth. Environ Microbiol 8:1–10

Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M(2010) Wheat (Triticum aestivum L.) growth enhancement byAzospirillum spp. under drought stress. World J MicrobiolBiotechnol 27:197–205

Benizri E, Amiaud B (2005) Relationship between plants and soilmicrobial communities in fertilized grasslands. Soil Biol Bio-chem 37:2055–2064

Berg G (2009) Plant–microbe interactions promoting plant growth andhealth: perspectives for controlled use of microorganisms inagriculture. Appl Microbiol Biotechnol 84:11–18

Berg G, Smalla K (2008) Plant species and soil type cooperativelyshape the structure and function of microbial communities in therhizosphere. FEMS Microbiol Ecol 68:1–13

Bianciotto V, Lumini E, Lanfranco L, Minerdi D, Bonfante P, PerottoS (2000) Detection and identification of bacterial endosymbiontsin arbuscular mycorrhizal fungi belonging to the family Giga-sporaceae. Appl Environ Microbiol 66:4503–4509

Böhme L, Böhme F (2006) Soil microbiological and biochemicalproperties affected by plant growth and different long-termfertilization. Europ J Soil Biol 42:1–12

Bonfante P (2003) Plants, mycorrhizal fungi, and endobacteria: adialog among cells and genomes. Biol Bulletin 204:215–220

Canbolat MY, Bilen S, Cakmakci R, Sahin F, Aydin A (2006) Effectof plant growth-promoting bacteria and soil compaction onbarley seedling growth, nutrient uptake, soil properties andrhizosphere microflora. Biol Fert Soils 42:350–357

Carlier E, Rovera M, Rossi J, Rosas SB (2008) Improvement ofgrowth, under field conditions, of wheat inoculated withPseudomonas chlororaphis subsp. aurantiaca SR1. World JMicrobiol Biotechnol 24:2653–2658

Chebotar VK, Makarova NM, Shaposhnikov AI, Kravchenko LV (2009)Antifungal and phytostimulating characteristics of Bacillus subtilisCh-13 rhizospheric strain, producer of bioprepations. ApplBiochem Microbiol 45:419–423

Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes,and soil organic matter decomposition. Plant Soil 202:167–174

Choi O, Kim J, Kim J-G, Jeong Y, Moon J, Park C, Hwang I (2008)Pyrroloquinoline quinone is a plant growth promotion factorproduced by Pseudomonas fluorescens B161. Plant Physiol146:657–668

Compant S, van der Heijden M, Sessitsch A (2010) Climate changeeffects on beneficial plant microorganism interactions. FEMSMicrobiol Ecol 73:197–214

Cruz A, Hamel C, Hanson K, Selles F, Zentner R (2009) Thirty-sevenyears of soil nitrogen and phosphorus fertility managementshapes the structure and function of the soil microbial communityin a Brown Chernozem. Plant Soil 315:173–184

Daei G, Ardakani M, Rejali F, Teimuri S, Miransari M (2009)Alleviation of salinity stress on wheat yield, yield components,and nutrient uptake using arbuscular mycorrhizal fungi underfield conditions. J Plant Physiol 166:617–625

Elcoka E, Kantar F, Sahin F (2008) Influence of nitrogen fixing andphosphorus solubilizing bacteria on the nodulation, plant growth,and yield of chickpea. J Plant Nutr 31:157–171

Emmerling C, Schloter M, Hartmann A, Kandeler E (2002)Functional diversity of soils organisms—a review of recentresearch activities in Germany. J Plant Nutr Soil Sci165:408–420

Flessa H, Ruser R, Dörsch P, Kamp T, Jimenez MA, Munch JC, BeeseF (2002) Integrated evaluation of greenhouse gas emissions(CO2, CH4, N2O) from two farming systems in southernGermany. Agric Ecosys Environ 91:175–189

George T, Gregory P, Hocking P, Richardson A (2008) Variation inroot associated phosphatase activities in wheat contributes to theutilization of organic P substrates in vitro, but does not explaindifferences in the P-nutrition when grown in soils. Environ ExpBot 64:239–249

Glick BR, Penrose DM, Li J (1998) A model for the lowering of plantethylene concentrations by plant growth promoting bacteria. JTheor Biol 190:63–68

Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR:commonalities and distinctions in the plant–bacterium signalingprocesses. Soil Biol Biochem 37:395–412

Gryndler M (2000) Interactions of arbuscular mycorrhizal fungi withother soil organisms. In: Kapulnik Y, Douds DDJ (eds)Arbuscular mycorrhizas: physiology and function. KluwerAcademic Press, Dordrecht, pp 239–262

Haas D, Défago G (2005) Biological control of soil borne pathogensby fluorescent pseudomonads. Nature Rev Microbiol 3:307–319

Han H, Lee K (2005) Physiological responses of soybean-inoculationof Bradyrhizobium japonicum with PGPR in saline soil con-ditions. Res J Agric Biol Sci 1:216–221

Harrier LA (2001) The arbuscular mycorrhizal symbiosis: a molecularreview of the fungal dimension. J Exp Bot 52:469–478

He K, Nukada H, Urakami T, Murphy MP (2003) Antioxidant andprooxidant properties of pyrroloquinoline quinone (PQQ): impli-cations for its function in biological system. Biochem Pharmacol65:67–74

Appl Microbiol Biotechnol (2011) 92:875–885 883

Hildebrandt U, Janetta K, Bothe H (2002) Towards growth ofarbuscular mycorrhizal fungi independent of a plant host. ApplEnviron Microbiol 68:1919–1924

Hodge A, Campbell CD, Fitter HA (2001) An arbuscular mycorrhizalfungus accelerates decomposition and acquires nitrogen directlyfrom organic material. Nature 413:297–299

Jalili F, Khavazi K, Pazira E, Nejati A, Asadi Rahmani H, RasuliSadaghiani H, Miransari M (2009) Isolation and characterizationof ACC deaminase producing fluorescent pseudomonads, toalleviate salinity stress on canola (Brassica napus L.) growth. JPlant Physiol 166:667–674

Kuiper I, Bloemberg GV, Lugtenberg BJJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclicaromatic hydrocarbon-degrading bacteria. Mol Plant MicrobeInteract 14:1197–1205

Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004)Rhizoremediation: a beneficial plantmicrobe interaction. MolPlant-Microbe Interact 17:6–15

Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization ofsoybean-associated bacteria and their potential for plant growthpromotion. Environ Microbiol 6:1244–1251

Kumazawa T, Sato K, Seno H, Ishii A, Suzuki O (1995) Levels ofpyrroloquinoline quinone in various foods. Biochem J 307:331–333

Liao M, Hocking P, Dong B, Delhaize E, Richardson A, Ryan P(2008) Variation in early phosphorus-uptake efficiency amongwheat genotypes grown on two contrasting Australian soils. AustJ Agric Res 59:157–166

Lugtenberg BJJ, Bloemberg GV (2004) Life in the rhizosphere.In: Ramos JL (ed) Pseudomonas, vol 1. Kluwer Academic/Plenum Publishers, New York, pp 403–430

Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria.Annu Rev Microbiol 63:541–556

Luo S, Wan Y, Xiao X, Guo H, Chen L, Xi Q, Zeng G, Liu C, Chen J(2011) Isolation and characterization of endophytic bacteriumLRE07 from cadmium hyperaccumulator Solanum nigrum L. andits potential for remediation. Appl Microbiol Biotechnol89:1637–1644

Lynch J (2005) Root architecture and nutrient acquisition. In:BassiriRad H (ed) Nutrient acquisition by plants: an ecologicalperspective. Springer, Berlin, pp 147–183

Ma J, Li XL, Xu H, Han Y, Cai ZC, Yagi K (2007) Effects of nitrogenfertilizer and wheat straw application on CH4 and N2O emissionsfrom a paddy rice field. Aust J Soil Res 45:359–367

Martinez-Romero E, Wang ET (2000) Sesbania herbacea–Rhizobiumhuautlense nodulation in flooded soils and comparative character-ization of S. herbaces nodulating rhizobia in different environ-ments. Microb Ecol 41:25–32

Miller S, Liu J, Allan D, Menzhuber C, Fedorova M, Vance C (2001)Molecular control of acid phosphatase secretion into therhizosphere of proteoid roots from phosphorus-stressed whitelupin. Plant Physiol 127:594–606

Miransari M (ed) (2011a) Soil nutrients. Nova, New York. ISBN 978-1-61324-785-3

Miransari M (2011b) Interactions between arbuscular mycorrhizalfungi and soil bacteria. Appl Microbiol Biotechnol 89:917–930

Miransari M, Mackenzie AF (2010) Wheat (Triticum aestivum L.)grain N uptake as affected by soil total and mineral N, for thedetermination of optimum N fertilizer rates for wheat production.Comm Soil Sci Plant Anal 41:1644–1653

Miransari M, Mackenzie AF (2011a) Development of a soil N-test forfertilizer requirements for corn (Zea mays L.) production inQuebec. Comm Soil Sci Plant Anal 42:50–65

Miransari M, Mackenzie AF (2011b) Development of a soil N test forfertilizer requirements for wheat. J Plant Nutr 34:762–777

Miransari M, Smith DL (2007) Overcoming the stressful effects ofsalinity and acidity on soybean [Glycine max (L.) Merr.]nodulation and yields using signal molecule genistein under fieldconditions. J Plant Nutr 30:1967–1992

Miransari M, Smith DL (2008) Using signal molecule genistein toalleviate the stress of suboptimal root zone temperature onsoybean-Bradyrhizobium symbiosis under different soil textures.J Plant Interact 3:287–295

Miransari M, Smith D (2009) Alleviating salt stress on soybean (Glycinemax (L.) Merr.)-Bradyrhizobium japonicum symbiosis, usingsignal molecule genistein. Europ J Soil Biol 45:146–152

Miransari M, Bahrami HA, Rejali F, Malakouti MJ, Torabi H (2007)Using arbuscular mycorrhiza to reduce the stressful effects of soilcompaction on corn (Zea mays L.) growth. Soil Biol Biochem39:2014–2026

Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Usingarbuscular mycorrhiza to reduce the stressful effects of soilcompaction on wheat (Triticum aestivum L.) growth. Soil BiolBiochem 40:1197–1206

Miransari M, Rejali F, Bahrami HA, Malakouti MJ (2009a) Effects ofsoil compaction and arbuscular mycorrhiza on corn (Zea maysL.) nutrient uptake. Soil Till Res 103:282–290

Miransari M, Rejali F, Bahrami HA, Malakouti MJ (2009b) Effects ofarbuscular mycorrhiza, soil sterilization, and soil compaction onwheat (Triticum aestivum L.) nutrients uptake. Soil Till Res104:48–55

Nicol GW, Glover A, Prosser JI (2003) The impact of grasslandmanagement on archaeal community structure in upland pasturerhizosphere. Environ Microbiol 5:152–162

Pinton R, Varanini Z, Nannipieri P (2001) The rhizosphere as a site ofbiochemical interactions among soil components, plants, andmicroorganisms. In: Pinton R, Varanini Z, Nannipieri P (eds) Therhizosphere. Mercel Dekker, New York, pp 1–18

Principe A, Alvarez F, Castro M, Zachi L, Fischer S, Mori G, Jofr E(2007) Biocontrol and PGPR features in native strains isolatedfrom saline soils of Argentina. Curr Microbiol 55:314–322

Qin S, Xing K, Jiang J-H, Xu L-H, Li WJ (2011) Biodiversity,bioactive natural products and biotechnological potential ofplant-associated endophytic actinobacteria. Appl Microbiol Bio-technol 89:457–473

Quideau SA, Chadwick OA, Benesi A, Graham RC, Anderson MA(2001) A direct link between forest vegetation type and soilorganic matter composition. Geoderma 104:41–60

Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophicendophytes. Trends Microbiol 6:139–144

Richardson A, Peter A, Hocking P, Simpson R, George T (2009) Plantmechanisms to optimise access to soil phosphorus. Crop PastureSci 60:124–143

Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. NewPhytol 171:41–53

Rovira AD (1959) Root excretions in relation to the rhizosphereeffect. IV. Influence of plant species, age of plant, light,temperature, and calcium nutrition on exudation. Plant Soil11:53–64

Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei HX, Pare PW,Kloepper JW (2003) Bacterial volatiles emissions promotegrowth in Arabidopsis. Proc Nat Acad Sci USA 100:4927–4932

Salimpour S, Khavazi K, Nadian H, Besharati H, Miransari M (2010)Enhancing phosphorous availability to canola (Brassica napusL.) using P solubilizing and sulfur oxidizing bacteria. Aust JCrop Sci 4:330–334

Sasaki T, Yamomoto Y, Ezaki B, Katsuhara M, Ahn S, Ryan P,Delhaize E, Matsumoyo H (2004) A wheat gene encoding analuminium-activated malate transporter. Plant J 37:645–653

Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth,

884 Appl Microbiol Biotechnol (2011) 92:875–885

yield, and nutrient use efficiency of wheat (Triticum aestivum L.).Appl Microbiol Biotechnol 79:147–155

Stites TE, Mitchell AE, Rucker RB (2000) Physiological importanceof quinoenzymes and the O-quinone family of cofactors. J Nutr130:719–727

Sziderics A, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007)Bacterial endophytes contribute to abiotic stress adaptation inpepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202

Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizalhyphae depends on the form of N supplied. Plant Cell Environ28:1247–1254

Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006)Attachment of different soil bacteria to arbuscular mycorrhizalfungal extraradical hyphae is determined by hyphal vitality andfungal species. FEMS Microbiol Letters 254:34–40

Ton J, de Vos M, Robben C, Buchala A, Métraux J, van Loon L,Pieterse C (2002) Characterization of Arabidopsis enhanceddisease susceptibility mutants that are affected in systemicallyinduced resistance. Plant J 29:11–21

Verhagen B, Bas W, Verhagen W, Glazebrook J, Zhu T, Chang H, vanLoon L, Pieterse C (2003) The transcriptome of rhizobacteria-

induced systemic resistance in Arabidopsis. Mol Plant MicrobInteract 17:895–908

Vessey KV (2003) Plant growth promoting rhizobacteria as biofertlizers.Plant Soil 255:571–586

Warembourg FR, Estelrich HD (2001) Plant phenology and soilfertility effects on below-ground carbon allocation for an annual(Bromus madritensis) and a perennial (Bromus erectus) grassspecies. Soil Biol Biochem 33:1291–1303

Wouterlood M, Cawthray G, Scanlon T, Lambers H, Veneklaas E(2004a) Carboxylate concentrations in the rhizosphere of lateralroots of chickpea (Cicer arietinum) increase during plantdevelopment, but are not correlated with phosphorus status ofsoil or plants. New Phytol 162:745–753

Wouterlood M, Cawthray G, Turner S, Lambers H, Veneklaas E(2004b) Rhizosphere carboxylate concentrations of chickpea areaffected by genotype and soil type. Plant Soil 261:1–10

Yang J, Kloepper J, Ryu C (2009) Rhizosphere bacteria help plantstolerate abiotic stress. Trend Plant Sci 14:1–4

Zabihi HR, Savaghebi GR, Khavazi K, Ganjali A, Miransari M (2010)Pseudomonas bacteria and phosphorous fertilization, affectingwheat (Triticum aestivum L.) yield and P uptake undergreenhouse and field conditions. Acta Physiol Plant 33:145–152

Appl Microbiol Biotechnol (2011) 92:875–885 885