An Overview of Plant Growth Promoting Rhizobacteria (PGPR) for Sustainable Agriculture

  • Rifat Hayat
  • Iftikhar Ahmed
  • Rizwan Ali Sheirdil

Abstract

Soil bacteria beneficial to plant growth usually referred to as plant growth promoting rhizobacteria (PGPR), are capable of promoting plant growth by colonizing the plant root. The mechanisms of PGPR-mediated enhancement of crop growth includes (i) a symbiotic and associative nitrogen fixation; (ii) solubilization and mineralization of other nutrients; (iii) production of hormones e.g. auxin i.e. indole acetic acid (IAA), abscisic acid (ABA), gibberellic acid and cytokinins; (iv) production of ACC-deaminase to reduce the level of ethylene in crop roots thus enhancing root length and density; (v) ability to produce antagonistic siderophores, ß-1-3-glucanase, chitinases, antibiotics, fluorescent pigment and cyanide against pathogens and (vi) enhanced resistance to drought and oxidative stresses by producing water soluble vitamins niacin, thiamine, riboflavin, biotin and pantothenic acid. Increased crop production through biocontrol is an indirect mechanism of PGPR that results in suppression of soil born deleterious microorganisms. Biocontrol mechanisms involved in pathogen suppression by PGPR include substrate competition, antibiotic production, and induced systemic resistance in the host. PGPR can play an essential role in helping plants to establish and grow in nutrient deficient conditions. Their use in agriculture can favour a reduction in agro-chemical use and support ecofriendly crop production. Trials with rhizosphere-associated plant growth-promoting P-solubilizing and N2-fixing microorganisms indicated yield increase in rice, wheat, sugar cane, maize, sugar beet, legumes, canola, vegetables and conifer species. A range of beneficial bacteria including strains of Herbaspirillum, Azospirillum and Burkholderia are closely associated with rhizosphere of rice crops. Common bacteria found in the maize rhizosphere are Azospirillum sp., Klebsiella sp., Enterobacter sp., Rahnella aquatilis, Herbaspirillum seropedicae, Paenibacillus azotofixans, and Bacillus circulans. Similarly, strains of Azotobacter, Azorhizobium, Azospirillum, Herbaspirillum, Bacillus and Klebsiella can supplement the use of urea-N in wheat production either by BNF or growth promotion. The commonly present PGPR in sugarcane plants are Azospirillum brasilense, Azospirillum lipoferum, Azospirillum amazonense, Acetobacter diazotrophicus, Bacillus tropicalis, Bacillus borstelensis, Herbaspirillum rubrisubalbicans and Herbaspirillum seropedicae. Symbiotic N2-fixing bacteria collectively known as Rhizobia are currently classified into six genera; Rhizobium, Allorhizobium, Azorhizobium, Bradyrhizobium, Mesorhizobium and Sinorhizobium and 91 species. Their inoculation may increase nodulation and N2-fixation in legumes. All these Rhizobiumn spp. can minimize chemical N fertilizers by BNF, but only if conditions for expression of N2-fixing activity and subsequent transfer of N to plants are favourable. In this Chapter, PGPR role has been discussed in the process of crop growth promotion, their mechanisms of action and their importance in crop production on sustainable basis.

Keywords

PGPR BNF P-solubilization Phytohormones Biocontrol Cereals Sugarcane and legumes crops 

1 Introduction

Plant growth promoting rhizobacteria (PGPR) are capable of promoting plant growth by colonizing their roots and can play an essential role in helping plants to establish and grow in nutrient deficient conditions. Their use in crop production can reduce the agro-chemical use and support ecofriendly sustainable food production. Plant growth promotion by PGPR is due to root hair proliferation, root hair deformation and branching, increase in seedling emergence, early nodulation, nodule functioning, enhanced leaf surface area, vigor, biomass, increasing indigenous plant hormones levels, mineral and water uptake, promoted accumulation of carbohydrates and yield in various plant species (Podile and Kishore 2006). The demand of PGPR biofertilizers has been increasing day by day with increase in the importance of organic agriculture with minimum inputs of chemicals. The population of PGPR in rhizospheric soil varies and depends largely on crop species and soil health (Tilak et al. 2005). Numerous studies clearly indicated the positive effect of PGPR on growth of different crops at different agroecological boundaries. Trials with soil rhizospheric N2-fixing and P-solubilizing Bacillus species showed yield increase in wheat (de Freitas 2000), rice (Sudha et al. 1999), maize (Pal 1998), sugar beet (Çakmakçi et al. 2006), canola (de Freitas et al. 1997), and conifer species (Bent et al. 2002). One of the most important and oftenly reported PGPR is Bacillus polymyxa, also known as Paenibacillus polymyxa (Timmusk et al. 1999) with a range of properties, including P-solubilization (de Freitas et al. 1997), nitrogen fixation (Coelho et al. 2003); production of cytokinin (Timmusk et al. 1999), antibiotic (Rosado and Seldin 1993), hydrolytic enzymes (Nielson and Sorenson 1997), colonization hair and cortical cells (Shishido et al. 1999), and increased root and shoot growth of crops (Sudha et al. 1999). Some strains of Rhodobacter are known to fix N2 (Drepper et al. 2002), but extensive studies are needed to validate its ability to fix N2. Pseudomonas sp. effectively adapt to new environments and colonize winter wheat roots (Misko and Germida 2002) thus significantly increasing root dry weight in spring wheat (Walley and Germida 1997), yield in sugar beet (Çakmakçi et al. 2001), and promote the growth of spinach (Urashima and Hori 2003).

Sustainable agriculture production can be achieved by emphasizing the use of PGPR as biofertilizer inoculants (Schippers et al. 1995). Generally, bacteria promote plant growth in three different ways (Glick 1995, 2001): synthesizing growth promoting harmones for the plants (Dobbelaere et al. 2003), facilitating the uptake of nutrients from the soil (Çakmakçi et al. 2006), and lessening or preventing the plants from diseases (Saravanakumar et al. 2008). The indepth mechanisms involved in plant growth by PGPR are yet to be investigated (Dey et al. 2004). However, the possible explanations include (i) solubilization of mineral phosphates and mineralization of other nutrients (Richardson 2001; Banerjee and Yasmin 2002); (ii) a biological nitrogen fixation (Kennedy et al. 2004a, b); (iii) ability to produce hormones like auxin i.e. indole acetic acid (IAA) (Patten and Glick 2002), abscisic acid (ABA) (Dobbelaere et al. 2003), gibberellic acid and cytokinins (Dey et al. 2004); (iv) ability to produce ACC-deaminase to reduce the level of ethylene in root of developing plants thereby increasing the root length and growth (Li et al. 2000; Penrose and Glick 2001); (v) antagonism against phytopathogenic bacteria by producing siderophores, ß-1,3-glucanase, antibiotics, chitinases, fluorescent pigment and cyanide (Glick and Pasternak 2003); and (vi) mediated resistance to drought (Alvarez et al. 1996) and oxidative stresses (Stajner et al. 1995, 1997) and production of water soluble vitamins thiamine, niacin, pantothenic acid, biotin and riboflavin (Revillas et al. 2000).

2 Biological Nitrogen Fixation (BNF)

Nitrogen is the most important nutrient and its deficiency severely affects crop yields. Most of the soils around globe are deficient in nitrogen and applications of nitrogenous fertilizer are essential for achieving maximum crop yield. Nitrogen is required for all living organisms. Although 78% of the atmosphere consists of dinitrogen, but it cannot be used by most organisms and consequently the availability of nitrogen in a form suitable for assimilation is often a major limiting factor for crop growth. The production of chemical nitrogen fertilizers not only depletes non-renewable energy resources but also poses human and environmental hazards, besides being very expensive. Urea is the cheapest and readily available N source, but unfortunately less than 50% of the applied urea is used by plants. This low efficiency of use is mainly caused by NH3 volatilisation and denitrification, and losses from leaching. Leaching of NO3-N causes ground water toxicity. Volatilisation and denitrification pollute the atmosphere through the evolution of greenhouse gases like N2O, NO and NH3. BNF not only complements and substitutes the mineral fertilizers but can be an economically beneficial and ecologically sound alternative (Glick et al. 1999).

BNF is a major source of nitrogen for plants as a part of environment friendly agricultural practices. It contributes for 65% of the total nitrogen currently utilized in crop production and will be important contributor for future agriculture (Matiru and Dakora 2004). This fixation is an important biochemical reaction next to plant photosynthesis for life on earth and occurs through symbiotic N2-fixing bacteria possessing the nitrogenase enzyme and in association with legumes (and some woody species) that converts atmospheric elemental dinitrogen (N2) into ammonia (Shiferaw et al. 2004). The potential of nitrogen fixation for most legumes species is in the range of 200–300 kg N ha−1 crop−1 (Peoples et al. 1995).

In the recent years, use of biological inoculants for sustainable crop production is attaining popularity in various parts of the world and biological nitrogen fixation represents the major source of N input in agricultural soils including those in arid regions. Symbiotic nitrogen-fixing bacteria include the cyanobacteria, the genera Rhizobium, Azorhizobium, Bradyrhizobium, Sinorhizobium, Allorhizobium, Mesorhizobium and Frankia (Paul and Clark 1996; Brock et al. 2000). The mechanisms of symbiotic N2-fixation between Rhizobium and legumes has been studied intensively. The symbiosis between Frankia and non-leguminous actinorhizal plants, is also been investigated now a days. Symbiotic system is the major N2-fixation system, playing a significant role in improving the fertility and maximizing productivity of low-N soils. Biological N2-fixed through rhizobium-legume symbiosis can also be beneficial to cereals growing in intercrops or to subsequent crops rotated with legumes. In many natural grassland systems, the grasses use N2 fixed by their legume counterparts for their nitrogen requirement and the protein available through this association enhances the forage quality for livestock production (Paynel et al. 2001). In addition to symbiotic N2-fixation in legumes, rhizobia as PGPR are also capable of contributing to growth promotion in non-legume species (Hoflich 2000). To act as PGPR, rhizobia naturally produce molecules (auxins, abscisic acids, cytokinins, riboflavin, lumichrome, lipo-chitooligosaccharides and vitamins) that promote crop growth, and their colonization and infection of cereal root would be expected to increase vigor and grain yield (Matiru and Dakora 2004). Other PGPR role of Rhizobium includes their ability to produce phytohormones (Arshad and Frankenberger 1998), solubilization of inorganic phosphorus (Chabot et al. 1996), siderophore release (Plessner et al. 1993; Jadhav et al. 1994) and antagonism against plant pathogenic microorganisms (Ehteshamul-Haque and Ghaffar 1993). Application of rhizobium inoculants under rainfed conditions on legumes like guar (Cyamopsis tetragonoloba L. Taub), moth (vigna acontifolia), mung (vigna ­radiate), and mash (vigna mungo) give up to 10–25% yield benefits (Rao 2004; Hayat et al. 2008a, b).

Free living bacteria as well as rhizobial strains can promote the growth of cereals by contributing to N-economy through their ability to fix N2 (Zahir et al. 2004). It is reported that biological N2-fixed by the diazotrophic PGPR may be a contributing factor of rice growth promotion in addition to other mechanisms (Biswas et al. 2000). Kennedy and Islam (2001) also explained the possible role and mechanisms of non-symbiotic bacteria to crop growth from BNF view point. Providing the plant with essential nutrients, e.g. NH4-N through atmospheric nitrogen fixation or aiding the plant in nutrient uptake is also considered as direct plant growth promotion. The important free living and associative nitrogen fixing genera are; Azospirillum, Azotobacter, Acetobacter (also known as Gluconacetobacter) Azoarcus, Achromobacter, Bacillus, Burkholderia, Clostridia, Citrobacter, Enterobacter, Herbaspirillum, Kelbsiella, Mycobacterium, Pseudomonas, Rhodobacter and Serratia. This list is increasing day by day.

3 Mineral-Solubilization and Uptake

PGPR directly contribute to the plant growth by facilitating plant nutritions through solubilization of inorganic phosphates and production of iron chelating siderophores thus increasing phosphorous and iron uptake.

3.1 Phosphorus Solubilization

Phosphate-solubilizing bacteria (PSB) could play an important role in supplying phosphate to plants in a more environment friendly and sustainable manner. The naturally abundant PSB solubilize Calcium-bound phosphatic compounds in an alkaline soil environment and convert the insoluble phosphatic compounds into soluble forms and make them available to crop plants. PSB are widely applied in agronomic practices in order to increase the productivity of crops while maintaining the health of soils. The beneficial effects of PSB on plant growth vary significantly depending on environmental conditions, bacterial strains, plant and soil conditions (Şahin et al. 2004; Çakmakçi et al. 2006). Various bacterial species in the genera Bacillus, Rhizobium and Pseudomonas, have proven to be the most powerful phosphate-solubilizing bacteria (Banerjee et al. 2006). There are also reports of phosphate solubilization by non-symbiotic nitrogen fixer, Azotobacter (Kumar et al. 2001). The phosphate-solubilizing activity of Rhizobium (e.g., Rhizobium/Bradyrhizobium) is associated with the production of 2-ketogluconic acid, indicating that phosphate-solubilizing activity of the organism is entirely due to its ability to reduce pH of the medium (Halder and Chakrabarty 1993). The phosphate-solubilizing ability also depends on nature of nitrogen source used in the media, with greater solubilization in presence of ammonium salts than when nitrate is used as nitrogen source. This has been attributed to extrusion of protons to compensate for ammonium uptake, leading to a decreased extra-cellular pH (Roos 1984). In some cases, however, ammonium can lead to decrease in phosphorus solubilization (Reyes et al. 1999). Several strains of P-solubilizers have been identified in vitro as Bacillus brevis, B. megaterium, B. polymyxa, B. sphaericus, B. thuringiensis and Xanthomonas maltophilia (de Freitas et al. 1997). P-solubilizing bacteria of Bacillus and Paenibacillus (formerly Bacillus) sp. have been applied to soils to successfully enhance the phosphorus status of plants (van Veen et al. 1997).

Since 1950s it is reported that P-solubilizing bacteria release phosphorus from organic and inorganic soil phosphorus pools through mineralization and solubilization (Fig. 22.1; Khan et al. 2009). Lowering of soil pH by microbial production of organic acids such as acid phosphatases, lactate, citrate, and succinate gluconic and keto gluconic acids etc. (Goldstein 1995; Deubel et al. 2000) and proton extrusion is the main principal mechanism of mineralization of organic form of phosphorus. Release of phosphorus from insoluble and adsorbed forms is also an important aspect of phosphorus solubilizing bacteria regarding phosphorus availability in soils. Phosphorus solubilizing bacteria transform soil phosphorus to forms that can easily be taken up by crops. Bacteria assimilate soluble phosphorus, and make it available by preventing it from adsorption (Khan and Joergensen 2009). Bacteria also enhance phosphorus availability to crops by solubilizing precipitated forms of phosphorus (Chen et al. 2006).
Fig. 22.1

Schematic diagram of soil phosphorus mobilization and immobilization by bacteria (Khan et al. 2009)

Fe - and Al - P and Ca - P are the main precipitated forms in acidic and alkaline soils respectively and can be solubilized involving organic anions and associated protons. Complex form of adsorbed phosphorus my be released by chelating metal ions through ligand exchange reactions. Soil bacteria use carbon and serve as a sink for phosphorus by immobilizing it from soil (Bünemann et al. 2004). Phosphorus solubilizing bacteria mainly depend on soil phosphorus and organic matter contents and release phosphorus from their cells for crops (Kim et al. 1998a). Agricultural and range land soils are main habitat of phosphorus solubilizing bacteria (Yahya and Azawi 1998) and their use in crop production can reduce chemical P by 50% without any significant reduction of crop yield (Yazdani et al. 2009). PSB biofertilizers have great potential for sustaining crop yield along with optimized phosphorus fertilization. Examples of P-solubilizing PGPR include Azotobacter chroococcum (Kumar and Narula 1999) and Bacillus circulans in wheat (Singh and Kapoor 1998), Enterobacter agglomerans in tomato (Kim et al. 1998b), Pseudomonas chlororaphis or Pseudomonas putida in soybean (Catellan et al. 1999) and other prominent P-solubilizing genera are Klebsiella, Balkhurdaria and Azospirillum etc. The availability of nutrients i.e. C, N and metals ions are the determining factors of P-solubilizing ability of PGPR. The activity of P-solubilizing rhizobacteria varies with nitrogen source and increases in the presence of low levels of Ca2+ and EDTA (Nautiyal et al. 2000). Soil bacteria could increase the P nutrition of plants through increased solubility of Ca-phosphates. Phosphate solubilization is the result of combined effect of pH decrease and production of organic acids (Fankem et al. 2006). Bacteria through secretion of different types of organic acids e.g. carboxylic acid and rhizospheric pH lowering mechanisms (He and Zhu 1988) dissociate the bound forms of phosphate like Ca3(PO4)2. Nevertheless, buffering capacity of the medium reduce the effectiveness of PSB in releasing P from tricalcium phosphates (Stephen and Jisha 2009). Acidification due to proton substitution/excretion of H+ (accompanying greater absorption of cations than anions) or release of Ca2+ by microbial population releases P from apatite (Goldstein 1994; Villegas and Fortin 2002). The reverse phenomenon become operative when uptake of anions increases than that of cations, with excretion of OH/HCO3 (Tang and Rengel 2003). PSB produce carboxylic anions, which have high affinity to calcium. This phenomenon results in more solubilization of phosphorus than acidification alone (Staunton and Leprince 1996). Complexation favoured by organic acids results in cations complexing structures in P solubilization, which is an important mechanism. Decrease in pH as well as synthesis of carboxylic acids results in the release of calcium phosphate (Ca-P); however, release of protons cannot be the single mechanism (Deubel et al. 2000). Crop yields improve with increased solubilization of the fixed soil P as well as the applied phosphates by PSB (Gull et al. 2004).

Most annual crops often do not get benefitted by direct application of phosphate rock in a short time. Phosphatic rocks can be solubilized by acid producing microorganisms (Gyaneshwar et al. 2002) to release more P for plant uptake. The inorganic P-solubilizing activities by PSB ranges between 25 and 42 μg P mL−1, whereas the organic P mineralization may occur between 8 and 18 μg P mL1 (Tao et al. 2008). The application of P fertilizers can be reduced by 25% and 50%, by using PSB inocula along with single super phosphate and rock phosphate, respectively (Sundara et al. 2002). It is reported that 29–62% P can be released by Pseudomonas putida, P. fluorescens Chao and P. fluorescens Tabriz; along with highest value of 0.74 mg P/50 mL from Fe2O3 (Ghaderi et al. 2008). Pseudomonas fluorescens is very effective and can solubilize 100 mg P L−1 containing Ca3(PO4)2 or 92 and 51 mg P L−1 containing AlPO4 and FePO4, respectively (Henri et al. 2008). Rock phosphatic minerals are often insoluble to provide sufficient P for plant uptake; however, using PSBs can release P from the fixed insoluble minerals and thus help to increase crop yields (Zaidi 1999). PGPR not only improves BNF but also contribute in increasing the availability of soluble P and thus, enhance plant growth (Ponmurugan and Gopi 2006). It is reported that PSB enhanced seedling length of Cicer arietinum (Sharma et al. 2007) and increase sugarcane yield (Sundara et al. 2002). Co-inoculation of PSB and PGPR can reduce application of P fertilizers by 50% without affecting corn yield (Yazdani et al. 2009). Grain yield of wheat increased 20–40% by the application of inoculation along with P fertilizers against sole P fertilization (Afzal and Bano 2008). The indigenous PSB populations often are not effective in releasing P from bound phosphates mainly due to high buffering capacity of soil; however, inoculants of PSB biofertilizers may contribute considerably in more plant P uptake. Plant available P increased by the activity of PSB especially belonging to the genera: Bacillus, Pseudomonas and Enterobacter. So, PSB has enormous potential in biofertilizer formulations to be exploited in increasing crop yields by increasing fixed P in the soil, as well as by making good use of natural reserves of phosphate rocks.

3.2 Iron Uptake

Iron being essential micronutrient of plants plays a key role in several enzymes with redox activity. Its role is important in photosynthesis, NO2 and SO4 reduction and N2 assimilation, and is therefore indispensable for chlorophyll biosynthesis (Rashid 1996). Iron is essential component of different steps involved in biosynthetic pathways and formation of chlorophyll required physiologically available iron to the plant (Lopez-Millan et al. 2001). Catalase and peroxidase are considered as important protoheme enzymes which can be used as biological markers in iron acquisition studies. Around 30% of the agronomic crops growing around the globe are facing the problem of chlorosis due to iron deficiency (Imsande 1998). Total soil Fe is always in excess of crop requirements, which is present in highly insoluble form of ferric hydroxide. In nature, various forms of iron are present in abundance but remain unavailable to plants due to their different solubility and bioavailability behaviour. The amount of soluble Fe in soil is much less than the total Fe contents thus iron remains unavailable for crops even in iron rich soils and contributes little in crop production (Podile and Kishore 2006). When iron availability to crops is inadequate for growth, leaves become pale green, yellow or white and eventually brown (Brittenham 1994). The availability of iron in soil solution is 10–18 M, a concentration even not sufficient for sustaining microbial growth. A large number of soil bacteria produce siderophores that bind Fe3+ and help in iron uptake (Podile and Kishore 2006). These siderophores can be used by rhizosphere bacteria and crops can absorb bacterial Fe3+ siderophore complexes. This mechanism is involved in iron absorption by crops especially in calcareous soils. Different kind of PGPR produce different kinds of siderophores. Pseudomonads are leading siderophore producers among PGPR and siderophore producing strains of fluorescent psuedomonas may be inoculated in calcareous soils for solubilization of non-available forms of iron (Sharma and Johri 2003).

Siderophores are iron chelating compounds having low molecular weight which are released under iron limited rhizospheric soils. These siderophores possess high binding affinity and specificity for iron (III) and help to facilitate its bioavailability into the biological cell (Schalk et al. 2001). The transportation of ferric siderophore complexes is a heterologous uptake and mediated by specific receptor proteins (Meyer et al. 2000). PGPR with the ability to produce siderophore play a vital role for iron acquisition in rhizo spheric soil. It is reported that under non-sterile soil system, crops show no iron-deficiency symptoms and have more iron uptake in roots as compared to crops grown in sterile soil (Masalha et al. 2000). This supports the possible role of PGPR in iron acquisition. Iron is present in different complexes each having different solubilities in natural system; therefore, the bioavailability of iron depends upon the potential of siderophores to chelate the iron from its complexes (Hersman et al. 2001). A cold-tolerant mutant of Pseudomonas fluorescens with 17-fold increase in siderophore production enhances colonization and PGP effect on mungbean (Katiyar and Goel 2004). Similarly, seed inoculation of maize with siderophore-producing Pseudomonas Pseudomonas chlororaphis enhances seed germination and root shoot biomass (Sharma and Johri 2003). Siderophores producing PGPR suppressed root pathogens by consuming available soil iron (Kloepper et al. 1980) and with the addition/availability of iron even in acidic soils (pH  <  6.0), these siderophores becomes less effective (Neilands and Nakamura 1991). Different bacterial proteins are involved in iron uptake and transport. This uptake by different bacterial species depends on the available concentration of soil iron.

4 Plant Growth Regulators

PGPR synthesize and export phytohormones also called as plant growth regulators (PGRs), that may be synthesized in defined organs of plant and can be translocated to other sites, where these trigger specific biochemical, physiological, and morphological role in plant growth and development (Hayat et al. 2011). PGRs are organic in nature that promote physiological processes of plants even at low concentrations and also take part in the development of tissues where they are produced. Among PGRs, gibberellins, cytokinins, auxins, abscisic acid and ethylene are well documented. The most common and active auxin in plants is indole-3-acetic acid (IAA), that regulates many aspects of plant growth and development throughout the plant cell cycle, from cell division, cell elongation and differentiation to root initiation, apical dominance, tropistic responses, flowering, fruit ripening, senescence and stimulation of plant growth. Regulation of these processes by auxin is believed to involve auxin-induced changes in gene expression (Guilfoyle et al. 1998). In addition to IAA, bacteria such as Paenibacillus polymyxa and Azospirillum also release other compounds in rhizosphere that could indirectly contribute to plant growth promotion like indole-3-butyric acid (IBA), Trp and tryptophol or indole-3-ethanol (TOL).

Cytokinins too are important phytohormones usually present in small amounts in biological samples (Vessey 2003). These enhance cell division, root development and root hair formation (Frankenberger and Arshad 1995), and are also involved in the processes such as photosynthesis or chloroplast differentiation. They are also known to induce opening of stomata, suppress auxin-induced apical dominance, and inhibit senescence of plant organs, especially in leaves (Crozier et al. 2001). More than 30 growth promoting compounds of cytokinin group are reported that are produced by plant associated PGPR. Cytokinin producing bacteria Azotobacter chroococcum and cytokinin precursor’s isopentyl alcohol (IA) and adenine (ADE) have been tested on maize crop under controlled and field conditions by Nieto and Frankenberger (1991). They observed improvement in crop growth. PGPR also produce widely recognized gibberellic acid (GA) and gibberellins (GAs).Over 89 GAs are known to date, most of which are primarily responsible for stem elongation (Dobbelaere et al. 2003). GAs also affect reproductive processes in a wide range of plants (Crozier et al. 2001). PGPR like Azospirillum and Pseudomonas sp. produce cytokinins and gibberellins (gibberellic acid). In addition to IAA, abscisic acid (ABA) has also been detected by radio-immunoassay or TLC in supernatants of Azospirillium sp. and Rhizobium sp. cultures (Dobbelaere et al. 2003).

Ethylene is a plant growth regulator synthesized by almost all species of bacteria (Primrose 1979). It acts as a ripening hormone, promotes adventitious root and root hair formation, stimulates germination, breaks dormancy of seeds; promote plant growth, development, and senescence. However, if ethylene concentration remains high after germination, root elongation, as well as symbiotic N2 fixation in leguminous plants is inhibited. PGPR produces enzyme like 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which hydrolyzes ACC and lowers the level of ethylene in crop rhizosphere. The product of this hydrolysis, ammonia and α-ketobutyrate, can be used by the bacterium as a source of nitrogen and carbon for growth. In this way the bacterium acts as a sink for ACC and thus lowers the ethylene level in plants, preventing some of the potentially deleterious consequences of high ethylene concentrations (Glick et al. 1998). PGPR with ACC-deaminase characteristics improve crop growth and yield and may be included bio-fertilizer biotechnology (Shaharoona et al. 2006). Role of PGPR in the production of phosphatase, β-glucanase, dehydrogenase and antibiotics has also been recognized. Another recently identified mechanism for plant growth promotion is due to production of volatiles by PGPR. Ryu et al. (2004) discussed in detail the role of bacterial volatiles in plant growth promotion in vitro. PGPR release different volatile blends and the differences in these volatile blends stimulate the plant growth. Volatile compounds like 3-hydroxy-2-butanone (acetoin) and 2,3-butanediol, produced by Bacillus subtilis and B. amyloliquefaciens stimulated the growth of Arabidopsis thaliana in in-vitro experiments. The volatile-mediated growth promotion by PGPR is by activation of cytokinin-signaling pathways.

5 Role of PGPR in Biocontrol Aspects

PGPR indirectly help in plant growth by suppression of deleterious microorganisms that inhibit plant growth or root pathogens through antibiosis, parasitism, competition for nutrients and space within the vicinity of plant roots, and/or activation of host defense responses (Podile and Kishore 2006). The strains of Bacillus subtilis are the most widely used PGPR due to their disease reducing and antibiotic producing capabilities (Kokalis-Burelle et al. 2006). Fluorescent pseudomonads are also known to suppress soil born fungal pathogens by producing antifungal metabolites and by sequestering iron in rhizosphere through the release of iron-chelating siderophores, rendering it unavailable to other organisms (Dwivedi and Johri 2003).

Suppression of deleterious microorganisms by PGPR is mainly by parasitism, by competing for available nutrients, production of enzymes or toxins and inducing resistance by activating plant defense response against pathogens (Podile and Kishore 2006). Fluorescent pseudomonads establish themselves on plant roots and sink the available nutrients, thus limiting the available nutrients required for the growth of pathogen (Walsh et al. 2001). PGPR also compete for nutrients with native rhizosphere microbes for elimination of pathogens. Siderophore production by PGPR, sequester most of available Fe3+ in the rhizosphere and force the pathogens for iron starvation, thus is a major contributor for pathogen suppression (O’Sullivan and O’Gara 1992). Suppression of Fusarium wilt of radish by Pseudomonas strain WCS358 through siderophore-mediated competition for iron (Costa and Loper 1994) is another example. Some PGPR’s degrade the cell wall of pathogenic fungi through production of hydrolytic enzymes (chitinase, β-1,3-glucanase). Purified chitinases of Bacillus subtilis AF 1 (Manjula et al. 2004), Serratia marcescens (Kishore et al. 2005b; Ordentlich et al. 1988) and S. plymuthica (Frankowski et al. 2001) are highly antifungal. β-1,3-glucanase producing strain of Pseudomonas cepacia inhibits the rhizosphere proliferation of various phytopathogenic fungi including Rhizoctonia solani, Sclerotium rolfsii and Pythium ultimum (Fridlender et al. 1993) and synergistic action of the two hydrolytic enzymes chitinases and β-1,3-glucanases was more effective in the inhibition of fungal pathogens than either enzyme alone (Tanaka and Watanabe 1995). Hydrolytic enzyme produced by pathogenic fungi includes pectolytic enzymes (polygalacturonases, pectin, lysis), cellulases and cutinase. PGPR’s inhibit (Podile and Kishore 2006) these pathogenic fungi and thus activity of these enzymes can be reduced with the reduction in virulence (Beraha et al. 1983). Bacillus megaterium B 153-2-2 inhibits the activities of extracellular enzymes, like cellulase, pectin lyase and pectinase produced by Rhizoctonia solani, by producing an extracellular endoproteinase (Bertagnolli et al. 1996). A groundnut seed endophytic bacterium Pseudomonas aeruginosa GSE 18, effective in control of groundnut stem rot disease, when applied as seed treatment or soil amendment, inhibits the production of cell wall-degrading enzymes (CWDE) polygalacturonase and cellulase by the pathogen Sclerotium rolfsii tested in vitro (Kishore et al. 2005c).A few strains of rhizobacteria activate plant defense responses against a broad spectrum of plant pathogens, termed as induced systemic resistance (ISR). Rhizobacteria-mediated ISR has been demonstrated in many plant-pathogen systems wherein the bacterium and the challenging pathogen remained spatially separated, and these observations indicate that ISR is genetically determined (Pieterse et al. 2001).

Inoculation of different strains of Pseudomonas fluorescens strains reduce the seedling mortality caused by Aspergillus niger (Dey et al. 2004) and show strong inhibition to Sclerotium rolfsii by reducing the incidence of stem rot severity. They also produce siderophores and antifungal metabolites. Production of antifungal metabolites by fluorescent Pseudomonads has been found to suppress soil-borne fungal pathogens on many occasions (Dey et al. 2004; Catellan et al. 1999). Similarly, Pseudomonas putida produces siderophores which convert a fusarium-conducive soil into a fusarium-suppressive soil for growth of different crops. Improvement in plant growth and disease resistance to a broad array of plant pests can be accomplished using PGPR (Kloepper et al. 2004). It is well recognized that PGPR can influence plant growth through creating resistance against pathogens. Bacillus subtilis is one such commercialized PGPR and it acts against a wide variety of pathogenic fungi (Banerjee et al. 2006).

6 Role of PGPR in Crop Production

Rice, wheat and maize are the three major staple food crops for world’s population. A variety of PGPR’s participate in interaction with C3 and C4 plants and can significantly increase their yield (Kennedy et al. 2004a, b). Rice crop removes around 16–17 kg N to produce 1 t dry weight of rice including straw. Wheat crop requires about 26–28 kg N to produce 1 t of grain including straw (Angus 2001). Maize plants require 9–11 kg N to produce 1 t biomass (Kennedy et al. 2004a, b). The N requirement of cereals is normally met by fertilization at a rate depending on soil fertility with chemical urea (Scharf 2001). PGPR inoculant biofertilizers can, in principle, be used to supplement or reduce the use of urea-N (Kennedy et al. 2004a, b). Those closely associated with rice rhizosphere are Azospirillum, Burkholderia and Herbaspirillum. A free living heterotrophic diazotroph like Azotobacter (A. vinelandii and A. chroococcum) uses C from sugar as energy source (Kennedy and Tchan 1992). There are obligatory anaerobic heterotrophs like Clostridia which are only capable of fixing N2 in the complete absence of oxygen (Kennedy and Tchan 1992; Kennedy et al. 2004a, b) and are usually isolated from rice fields (Elbadry et al. 1999). Their activity in rice may be enhanced with the addition of organic source like straw (Kanungo et al. 1997), presumably as a result of microbial breakdown of cellulose into cellobiose and glucose. Yield of rice can be increased with the application of Azotobacter, Azospirillum lipoferum and Azospirillum brasilense, Azospirillum (Reis et al. 2000). Similarly, Burkholderia vietnamiensis increases rice grain yields significantly up to 8 t ha−1 (Tran Vân et al. 2000) by supplementing 25–30 kg N ha−1 as synthetic fertilizer. Family Enterobacteriaceae has several diazotrophs like Klebsiella (K. pneumonia), Enterobacter (E. cloacae), Citrobacter (C. freundii), and Pseudomonas (Ps. putida or Ps. fluorescens) isolated from rice rhizosphere with plant growth promoting traits (Kennedy et al. 2004a, b). Another rice endophyte Herbaspirillum seropedicae (James et al. 2000) can fix upto 45% of total plant N in rice from the atmosphere (Baldani et al. 2000). The N2- fixation range by Herbaspirillum was assessed upto 58 mg tube−1 under aseptic conditions (Reis et al. 2000). Azoarcus sp. is also endophytic Gram-negative N2-fixing bacterium firstly isolated from Kallar grass (Leptochloa fusa Kunth) growing in saline-sodic soils of Pakistan (Reinhold-Hurek et al. 1993). Azoarcus colonise rice under both laboratory and field condition (Hurek et al. 1994; Reinhold-Hurek et al. 2002). Multi-strain biofertilizer (BioGro) containing three different PGPR like Pseudomonas (Ps. fluorescens, Ps. putida), Klebsiella (K. pneumonia) and Citrobacter (C. freundii) isolated from rice rhizospheric soil of Hanoi, Vietnam (Nguyen et al. 2003) significantly increased rice grain yield in Vietnam and Australia (Williams and Kennedy 2002). National Institute for Biotechnology and Genetic Engineering (NIBGE) of Pakistan also prepared a multi-strain rice biofertilizer rice with the commercial name “BioPower” (Malik et al. 2002) and similar product is also available in Egypt (Hegazi et al. 1998). These inoculants are claimed to give similar yield increases on rice farms upto 20% (Kennedy et al. 2004a, b).

Similarly, strains of Azospirillum, Azotobacter, Azorhizobium, Bacillus, Herbaspirillum and Klebsiella can supplement the use of urea-N in wheat production either by BNF or growth promotion (Kennedy and Islam 2001). The N requirement of wheat is higher than that for rice, because of its higher grain protein content. Wheat yields vary widely from 1 to 7 t ha−1 dependent on inherent soil fertility, amount of applied fertilizer, wheat variety, diseases, other management practices and environmental conditions (Angus 2001).Thus, estimated amount of N removed by wheat crop varies between 26 and 200 kg N ha−1, depending on the yield (Reeves et al. 2002). To maximize wheat yields in soils that are not capable of supplying enough N, chemical fertilizers such as urea are used to enhance N supply. Biofertilizers are also being used to supplement the use of urea worldwide. The estimated amount of BNF by such wheat-bacterial associations was between 10 and 30 kg N ha−1 (Kennedy and Islam 2001) or about 10% of their total-N requirement. Wheat transformed about 30% of carbon assimilates into the process of rhizodeposition and part of this below ground translocated C is incorporated by rhizosphere micro-organisms (Kuzyakov and Domanski 2000). Studies indicate that PGPR may act as natural elicitor for improving the growth and yield of wheat. Important PGPR responsible for increased wheat yield in different parts of world are Pseudomonas (ps. cepacia, ps. aeruginosa, ps. fluorescens and ps. putida, ps. chlororaphis), Bacillus (B. cereus), Azospirillum (A. brasilense, A. lipoferum) and Herbaspirillum (H. seropedicae). Common PGPR species found in rhizosphere of maize are Enterobacter sp., Rahnella aquatilis, Paenibacillus azotofixans, Herbaspirillum seropedicae, Bacillus circulans, Klebsiella sp. and Azospirillum sp. (Chelius and Triplett 2000). The positive effects of Azospirillum on maize growth are mainly derived from physiological changes of the inoculated plant roots, which enhance water and mineral nutrient uptake (Okan and Kapulnik 1986). Both Azospirillum brasilense and Azospirillum irakense are used as inoculant biofertilizer for maize. Other species of Azospirillum capable of increasing the yield of maize are A. lipoferum, and A. indigens. Azorhizobium caulinodans is also capable of giving such beneficial effects (Riggs et al. 2001). Herbaspirillium seropedicae can improve the ability of maize plant to use fertilizer N more efficiently and the yield increase due to H. seropedicae was up to 19.5% (Riggs et al. 2001). PGPR strains Burkholderia (B. cepacia), Pseudomonas (P. fluorescens), Serratia (S. proteamaculans, and S. liquefaciens), Rhizobium (R. etli bv. Phaseoli, R. leguminosarum bv. Trifolii) and Sinorhizobium sp. increase corn growth, plant height and grain yield of maize in different agro-ecological zones. The diazotrophs commonly present in sugarcane plants are Acetobactor also known as Gluconacetobacter (A. diazotrophicus), Azospirillum (A. brasilense, A. lipoferum, A. amazonense), Burkholderia (B. brasilensis, B. tropicalis), and Herbaspirillum (H. seropedicae, H. rubrisubalbicans) (Kennedy and Islam 2001). Sugarcane requires approximately 1.45 kg N ha−1 to produce 1 t moist biomass (Bhuiyan 1995) or about 7 kg N ha−1 for 1 t of dry cane. Generally 150–250 kg urea-N ha−1 is applied for sugarcane cultivation depending on soil fertility, genotype and the targeted yield. Evidence from Brazil indicates fertilizer-N of sugarcane can be reduced to half by exploiting BNF systems, claimed to be based on diazotrophic PGPR such as Acetobacter (Gluconacetobacter) and Herbaspirillum (Döbereiner 1997; Döbereiner and Baldani 1998). More than 70% of sugarcane N (200 kg N ha−1 y−1) was derived from biological fixed N2 by Azospirillum (A. diazotrophicus) (Boddey et al. 1991). Similarly, Acetobacter (with nifH+) -sugarcane system has also been well established (Lee et al. 2002). Azotobacter sp. and Klebsiella mobilis are reported for improving potato yield. Similarly Pseudomonas fluorescent and Achromobacter piechaudii increase tomato yield. Positive effect of PGPR (Bacillus cereus; Pseudomonas putida; Pseudomonas fluorescens; Serratia liquefaciens; Arthrobacteer cetreus; Escherichia coli, Mesorhizobium loti and Delftia acidovorans) inoculation on the growth and yield of rapeseed have been reported by many researchers. Burkholderia cepacia alone or in combination with Enterobacter spp. and Pseudomonas fluoroscens have also been tested for its ability to promote growth of sorghum (Sorghum bicolar) (Chiarini et al. 1998). Inoculation with effective bacterial strains (Pseudomonas alcaligenes, Pseudomonas denitrificans, Bacillus polymyxa, Azospirillum brasilense and Mycobacterium phlei) increases the root and shoot growth of cotton (Anjum et al. 2007). Çakmakçi et al. (2007) also conducted a study on barley under greenhouse conditions in order to investigate seed inoculation with five different N2-fixing (Bacillus licheniformis, Rhodobacter capsulatus, Paenibacillus polymyxa, Pseudomonas putida, and Bacillus spp. OSU-142) and two different phosphate-solubilising (Bacillus megaterium and Bacillus spp. M-13) bacteria in comparison to control and mineral fertiliser (N and P) application. Co-inoculation of legumes with PGPR and Rhizobium has received increasing attention in recent years. Co-inoculation with symbiotic bacteria and rhizosphere bacteria may increase nodulation through a variety of mechanisms. PGPR strains, from a range of genera, enhance legume growth, nodulation and nitrogen fixation when co-inoculated with their effective rhizobia. Examples of these are Azospirillum (A. lipoferum, A. brasilense), Azotobacter (A. chroococcum), Bacillus (B. cereus, B. endophyticus, B. pumilus, B. subtilis, B. firmis, B. megaterium), Paenibacillus (P. lautus, P. macerans, P. polymyxa,), Pseudomonos (Ps. fluorescens, Ps. putida, Ps. aeruginosa) Serratia (S. lequefacians, S. proteamaculans), Aeromonas hydrophia and, Streptomyces (Pal et al. 2004; Kishore et al. 2005a; Figueiredo et al. 2007) . All these bacteria including cyanobacteria can supplement urea-N by BNF, but only if conditions for expression of N2-fixing activity and subsequent transfer of N to plants are favourable. In general, it is believed that PGPR are more effective in promoting plant growth under limited supply of nutrients; however, present scenario does not allow to compromise on actual potential of crop productivity by reducing use of chemical fertilizers. Hence, it is of prime importance to isolate such PGPR strains that could be effective even under optimum nutrition. The biosynthesis of ethylene in plant roots is significantly affected by concentration of NO3-N present around the roots (Ligero et al. 1999). Higher levels of NO3 in rooting medium stimulate ACC-oxidase activity leading to increased ethylene production, which is generally believed to be inhibitory to root growth (Glick et al. 1998). The nitrogenous fertilizer applied in ammonical form is readily oxidized to NO3-N under aerobic conditions. It is very likely that NO3-N present in the vicinity of roots reduces the efficiency of PGPR by inducing ethylene synthesis. However, PGPR containing ACC-deaminase minimizes the NO3 induced ethylene synthesis.

7 Conclusion

PGPR are able to enhance significantly the yield of cereals, legumes and sugarcane crops etc. Soil and plant health can be enhanced through PGPR-crops rhizospheric interactions. From the agricultural viewpoint, the aim will be to increase the yield on sustainable basis, while maintaining soil health. To achieve this, knowledge about indigenous PGPR for different crop rhizospheric environment must be improved. It is also necessary to adopt and maintain minimal standards for production of PGPR inoculants/biofertilizers. PGPR biofertilizers not only promote crop growth but also enhance the resistance against pathogens. Integrated use of PGPR along with inorganic and organic nutrient sources provides a sustainable agricultural ecosystem.

References

  1. Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). Int J Agric Biol 10:85–88Google Scholar
  2. Alvarez MI, Sueldo RJ, Barassi CA (1996) Effect of Azospirillum on coleoptile growth in wheat seedlings under water stress. Cereal Res Commun 24:101–107Google Scholar
  3. Angus JF (2001) Nitrogen supply and demand in Australian agriculture. Aust J Exp Agric 41:277–288CrossRefGoogle Scholar
  4. Anjum MA, Sajjad MR, Akhtar N, Qureshi MA, Iqbal A, Jami AR, Hassan M (2007) Response of cotton to plant growth promoting rhizobacteria (PGPR) inoculation under different levels of nitrogen. J Agric Res 45(2):135–143Google Scholar
  5. Arshad M, Frankenberger WT Jr (1998) Plant growth regulating substances in the rhizosphere. Microbial production and function. Adv Agron 62:46–51Google Scholar
  6. Baldani VLD, Baldani JI, Dobereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillums seropidicae. Biol Fertil Soils 30:485–491CrossRefGoogle Scholar
  7. Banerjee MR, Yasmin L (2002) Sulfur oxidizing rhizobacteria: an innovative environment friendly soil biotechnological tool for better canola production. Proceeding of Agroenviron, 26–29 Oct 2002, Cairo, Egypt, pp 1–7Google Scholar
  8. Banerjee MR, Yesmin L, Vessey JK (2006) Plant growth promoting rhizobacteria as biofertilizers and biopesticides. In: Rai MK (ed) Handbook of microbial biofertilizers. Haworth Press, Inc., New YorkGoogle Scholar
  9. Bent E, Breuil C, Enebak S, Chanway CP (2002) Surface colonization of lodgepole pine (Pinus contorta var lati folia [Dougl. Engelm.]) roots by Pseudomonas fluorescens and Paenibacillus polymyxa under gnotobiotic conditions. Plant Soil 241:187–196CrossRefGoogle Scholar
  10. Beraha L, Wisniewski V, Garber ED (1983) Avirulence and reduced extracellular enzyme activity in Geotrichum candidum. Bot Gazette 144:461–465CrossRefGoogle Scholar
  11. Bertagnolli BL, Soglio FKD, Sinclair JB (1996) Extracellular enzyme profiles of the fungal pathogen Rhizoctonia solani isolate 2B-12 and of two antagonists, Bacillus megaterium strain B153-2-2 and Trichoderma harzianum isolate Th008. I. Possible correlations with inhibition of growth and biocontrol. Physiol Mol Plant Pathol 48:145–160CrossRefGoogle Scholar
  12. Bhuiyan NI (1995) Intensive cropping and soil nutrient balance in Bangladesh. In: Hussain MS, Huq SMI, Iqbal M, Khan TH (eds) Improving soil management for intensive cropping in the tropics and sub-tropics. Bangladesh Agricultural Research Council, Dhaka, pp 61–71Google Scholar
  13. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
  14. Boddey RM, Urquiaga S, Reis V, Döbereiner J (1991) Biological nitrogen fixation associated with sugar cane. Plant Soil 137:111–117CrossRefGoogle Scholar
  15. Brittenham GM (1994) New advances in iron metabolism, iron deficiency and iron overload. Curr Opin Hematol 1:549–556Google Scholar
  16. Brock JL, Albrecht KA, Tilbrook JC, Hay MJM (2000) Morphology of white clover during development from seed to clonal populations in grazed pastures. J Agric Sci 135:103–111CrossRefGoogle Scholar
  17. Bünemann EK, Bossio DA, Smithson PC, Frossard E, Oberson A (2004) Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol Biochem 36:889–901CrossRefGoogle Scholar
  18. Çakmakçi R, Kantar F, Şahin F (2001) Effect of N2-fixing bacterial inoculations on yield of sugar beet and barley. J Plant Nutr Soil Sci 164:527–531CrossRefGoogle Scholar
  19. Çakmakçi R, Dönmez F, Aydın A, Şahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487CrossRefGoogle Scholar
  20. Çakmakçi R, Erat M, Erdoğan ÜG, Dönmez MF (2007) The influence of PGPR on growth parameters, antioxidant and pentose phosphate oxidative cycle enzymes in wheat and spinach plants. J Plant Nutr Soil Sci 170:288–295CrossRefGoogle Scholar
  21. Catellan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680CrossRefGoogle Scholar
  22. Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321CrossRefGoogle Scholar
  23. Chelius MK, Triplett EW (2000) Diazotrophic endophytes associated with maize. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham, pp 779–791Google Scholar
  24. Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41CrossRefGoogle Scholar
  25. Chiarini L, Bevivino A, Tabacchioni S, Dalmastri C (1998) Inoculation of Burkholderia cepacia, Pseudomonas fluorescens and Enterobacter sp. on Sorghum bicolor: root colonization and plant growth promotion of dual strain inocula. Soil Biol Biochem 30:81–87CrossRefGoogle Scholar
  26. Coelho MRR, Weid I, von der Zahner V, Seldin L (2003) Characterization of nitrogen-fixing Paenibacillus species by polymerase chain reaction-restriction fragment length polymorphism analysis of part of genes encoding 16S rRNA and 23S rRNA and by multilocus enzyme electrophoresis. FEMS Microbiol Lett 222:243–250PubMedCrossRefGoogle Scholar
  27. Costa JM, Loper JE (1994) Characterization of siderophore production by the biological control agent Enterobacter cloacae. Mol Plant-Microb Interact 7:440–448CrossRefGoogle Scholar
  28. Crozier A, Kamiya Y, Bishop G, Yokota T (2001) Biosynthesis of hormones and elicitors molecules. In: Buchanan BB, Grussem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologists, Rockville, pp 850–900Google Scholar
  29. de Freitas JR (2000) Yield and N assimilation of winter wheat (Triticum aestivum., var Norstar) inoculated with rhizobacteria. Pedobiologia 44:97–104Google Scholar
  30. de Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soils 24:358–364CrossRefGoogle Scholar
  31. Deubel A, Gransee A, Merbach W (2000) Transformation of organic rhizodeposits by rhizoplane bacteria and its influence on the availability of tertiary calcium phosphate. J Plant Nutr Soil Sci 163:387–392CrossRefGoogle Scholar
  32. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L) by application of plant growth promoting rhizobacteria. Microbiol Res 159:371–394PubMedCrossRefGoogle Scholar
  33. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  34. Döbereiner J (1997) Biological nitrogen fixation in the tropics: social and economic contributions. Soil Biol Biochem 29:771–774CrossRefGoogle Scholar
  35. Döbereiner J, Baldani VLD (1998) Biological nitrogen fixation by endophytic diazotrophs in non-leguminous crops in the tropics. In: Malik KA, Mirza MS, Ladha JK (eds) Nitrogen fixation with non-legumes. Kluwer Academic Publishers, Dordrecht, pp 3–7CrossRefGoogle Scholar
  36. Drepper T, Raabe K, Giaourakis D, Gendrullis M, Masepohl B, Klipp W (2002) The Hƒq-like protein Nrƒa of the phototrophic purple bacterium Rhodobacter capsulatus controls ­nitrogen fixation via regulation of niƒA and anƒA expression. FEMS Microbiol Lett 215:221–227PubMedCrossRefGoogle Scholar
  37. Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: biosynthesis and regulation. Curr Sci 12:1693–1703Google Scholar
  38. Ehteshamul-Haque S, Ghaffar A (1993) Use of Rhizobia in the control of root diseases of sunflower, okra, soybean and mungbean. J Phytopathol 138:157–163CrossRefGoogle Scholar
  39. Elbadry M, El-Bassel A, Elbanna K (1999) Occurrence and dynamics of phototrophic purple nonsulphur bacteria compared with other asymbiotic nitrogen fixers in rice fields of Egypt. World J Microbiol Biotechnol 15:359–362CrossRefGoogle Scholar
  40. Fankem H, Nwaga D, Deubel A, Dieng L, Merbach W, Etoa FX (2006) Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr J Biotechnol 5:2450–2460Google Scholar
  41. Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2007) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 24(7):1187–1193CrossRefGoogle Scholar
  42. Frankenberger WTJ, Arshad M (1995) Photohormones in soil: microbial production and function. Deker, New York, p 503Google Scholar
  43. Frankowski J, Lorito M, Scala F, Schmid R, Berg G, Bahl H (2001) Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch Microbiol 176:421–426PubMedCrossRefGoogle Scholar
  44. Fridlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a β-1,3-glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221CrossRefGoogle Scholar
  45. Ghaderi A, Aliasgharzad N, Oustan S, Olsson PA (2008) Efficiency of three Pseudomonas isolates in releasing phosphate from an artificial variable-charge mineral (iron III hydroxide). Soil Environ 27:71–76Google Scholar
  46. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  47. Glick BR (2001) Phytoremediation: synergistic use of plants and bacteria to cleanup the environment. Biotechnol Adv 21(3):83–393Google Scholar
  48. Glick BR, Pasternak JJ (2003) Plant growth promoting bacteria. In: Glick BR, Pasternak JJ (eds) Molecular biotechnology – principles and applications of recombinant DNA, 3rd edn. ASM Press, Washington, DC, pp 436–454Google Scholar
  49. Glick BR, Penrose DM, Li J (1998) A model for lowering plant ethylene concentration by plant growth promoting rhizobacteria. J Theor Biol 190:63–68PubMedCrossRefGoogle Scholar
  50. Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London, 267ppCrossRefGoogle Scholar
  51. Goldstein AH (1994) Involvement of the quinoprotein glucose dehydrogenises in the solubilization of exogenous phosphates by gram-negative bacteria. In: Torriani A, Yagil GE, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 197–203Google Scholar
  52. Goldstein AH (1995) Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram-negative bacteria. Biol Agri Hortic 12:185–193CrossRefGoogle Scholar
  53. Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone responsive transcription. Cell Mol Life Sci 54:619–627PubMedCrossRefGoogle Scholar
  54. Gull M, Hafeez FY, Saleem M, Malik KA (2004) Phosphorus uptake and growth promotion of chickpea by co-inoculation of mineral phosphate solubilizing bacteria and a mixed rhizobial culture. Aust J Exp Agric 44:623–628CrossRefGoogle Scholar
  55. Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93CrossRefGoogle Scholar
  56. Halder AK, Chakrabarty PK (1993) Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol 38:325–330CrossRefGoogle Scholar
  57. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2011) Soil beneficial bacteria and their role in plant growth promotion. A Review. Ann Microbiol 60:579–598Google Scholar
  58. Hayat R, Ali S, Siddique MT, Chatha TH (2008a) Biological nitrogen fixation of summer legumes and their residual effects on subsequent rainfed wheat yield. Pak J Bot 40(2):711–722Google Scholar
  59. Hayat R, Ali S, Ijaz SS, Chatha TH, Siddique MT (2008b) Estimation of N2-fixation of mung bean and mash bean through xylem uriede technique under rainfed conditions. Pak J Bot 40(2):723–734Google Scholar
  60. He ZL, Zhu J (1988) Microbial utilization and transformation of phosphate adsorbed by variable charged minerals. Soil Biol Biochem 30:917–923CrossRefGoogle Scholar
  61. Hegazi NA, Faye M, Amin G, Hamza MA, Abbas M, Youssef H, Monib M (1998) Diazotrophs associated with non-legumes grown in sandy soil. In: Malik KA, Mirza MS, Ladha JK (eds) Nitrogen fixation with non-legumes. Kluwer Academic Publishers, Dordrecht, pp 209–222CrossRefGoogle Scholar
  62. Henri F, Laurette NN, Annette D, John Q, Wolfgang M, François-Xavier E, Dieudonné N (2008) Solubilization of inorganic phosphates and plant growth promotion by strains of Pseudomonas fluorescens isolated from acidic soils of Cameroon. Afr J Microbiol Res 2:171–178Google Scholar
  63. Hersman LE, Folsythe JH, Ticknor LO, Maurice PA (2001) Growth of Pseudomonas mendocina on Fe (III) (hydr) oxides. Appl Environ Microbiol 67:4448–4453PubMedCrossRefGoogle Scholar
  64. Hoflich G (2000) Colonization and growth promotion of non-legumes by Rhizobium bacteria. Micobial biosystems: new prontiers. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Proceedings of the 8th international symposium on microbial ecology, Atlantic Canada Society for Microbial Ecology, Halifax, Canada, pp 827–830Google Scholar
  65. Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176:1913–1923PubMedGoogle Scholar
  66. Imsande J (1998) Nitrogen deficit during soybean pod fill and increased plant biomass by vigorous N2 fixation. Eur J Agron 8(1–2):1–11CrossRefGoogle Scholar
  67. Jadhav RS, Thaker NV, Desai A (1994) Involvement of the siderophore of cowpea Rhizobium in the iron nutrition of the peanut. World J Microbiol Biotechnol 10:360–361CrossRefGoogle Scholar
  68. James EK, Gyaneshwar P, Barraquio WL, Mathan N, Ladha JK (2000) Endophytic diazotrophs associated with rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. International Rice Research Institute, Los Ban˜os, pp 119–140Google Scholar
  69. Kanungo PK, Panda D, Adhya TK, Ramakrishnan B, Rao VR (1997) Nitrogenase activity and nitrogen fixing bacteria associated with rhizosphere of rice cultivars. J Sci Food Agric 73:485–488CrossRefGoogle Scholar
  70. Katiyar V, Goel R (2004) Siderophore-mediated plant growth promotion at low temperature by mutant of fluorescent pseudomonad. Plant Growth Regul 42:239–244CrossRefGoogle Scholar
  71. Kennedy IR, Islam N (2001) The current and potential contribution of asymbiotic nitrogen requirements on farms: a review. Aust J Exp Agric 41:447–457CrossRefGoogle Scholar
  72. Kennedy IR, Tchan Y (1992) Biological nitrogen fixation in no leguminous field crops: recent advances. Plant Soil 141:93–118CrossRefGoogle Scholar
  73. Kennedy IR, Choudhury AIMA, KecSkes ML (2004a) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Boil Biochem 36(8):1229–1244CrossRefGoogle Scholar
  74. Kennedy N, Brodie E, Conolly J, Clipson N (2004b) Impact of lime, nitrogen and plant species on bacterial community structure in grassland microcosms. Environ Microbiol 6:1070–1080PubMedCrossRefGoogle Scholar
  75. Khan KS, Joergensen RG (2009) Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresour Technol 100:303–309PubMedCrossRefGoogle Scholar
  76. Khan AA, Jillani G, Akhtar MS, Naqvi SMS, Rasheed M (2009) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci 1(1):48–58Google Scholar
  77. Kim KY, Jordan D, McDonald GA (1998a) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fert Soils 26:79–87CrossRefGoogle Scholar
  78. Kim KY, Jordan D, McDonald GA (1998b) Enterobacter agglomerans, phosphate solubilizing bacteria, and microbial activity in soil: effect of carbon sources. Soil Biol Biochem 30:995–1003CrossRefGoogle Scholar
  79. Kishore GK, Pande S, Podile AR (2005a) Phylloplane bacteria increase seedling emergence, growth and yield of field-grown groundnut (Arachis hypogaea L.). Lett Appl Microbiol 40:260–268PubMedCrossRefGoogle Scholar
  80. Kishore GK, Pande S, Podile AR (2005b) Biological control of late leaf spot of peanut (Arachis hypogaea L.) with chitinolytic bacteria. Phytopathology 10:1157–1165CrossRefGoogle Scholar
  81. Kishore GK, Pande S, Rao JN, Podile AR (2005c) Pseudomonas aeruginosa inhibits the plant cell wall degrading enzymes of Sclerotium rolfsii and reduces the severity of groundnut stem rot. Eur J Plant Pathol 113(3):315–320CrossRefGoogle Scholar
  82. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886CrossRefGoogle Scholar
  83. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11):1259–1266PubMedCrossRefGoogle Scholar
  84. Kokalis-Burelle N, Kloepper JW, Reddy MS (2006) Plant growth-promoting rhizobacteria as transplant amendments and their effects on indigenous rhizosphere microorganisms. Appl Soil Ecol 31(1–2):91–100CrossRefGoogle Scholar
  85. Kumar V, Narula N (1999) Solubilization of inorganic phosphates and growth emergence of wheat as affected by Azotobacter chroococcum mutants. Biol Fert Soils 28:301–305CrossRefGoogle Scholar
  86. Kumar V, Behl RK, Narula N (2001) Establishment of phosphate solubilizing strains of Azotobacter chroococcum in the rhizosphere and their effect on wheat cultivars under greenhouse conditions. Microbiol Res 156:87–93PubMedCrossRefGoogle Scholar
  87. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. J Plant Nutr Soil Sci 163:421–431CrossRefGoogle Scholar
  88. Lee S, Pierson B, Kennedy C (2002) Genetics and biochemistry of nitrogen fixation and other factors beneficial to host plant growth in diazotrophic endophytes. In: Vanderleyden J (ed) Proceedings of the ninth international symposium on nitrogen fixation with nonlegumes, Katholique Universiteit, Leuven, Belgium, pp 41–42Google Scholar
  89. Li J, Ovakin DH, Charles TC, Glick BR (2000) An ACC deaminase minus mutant of Entreobacter cloacae UW4 no longer promotes root elongation. Curr Microbiol 41:101–105PubMedCrossRefGoogle Scholar
  90. Ligero F, Poreda JL, Gresshoff PM, Caba JM (1999) Nitrate inoculation is in enhanced ethylene biosynthesis in soybean roots as a possible mediator of nodulation control. J Plant Physiol 154:482–488CrossRefGoogle Scholar
  91. Lopez-Millan AF, Morales F, Abadia A, Abadia J (2001) Iron deficiency-associated changes in the composition of the leaf apoplastic fluid from field-grown pear (Pyrus communis) trees. J Exp Bot 52:1489–1498PubMedCrossRefGoogle Scholar
  92. Malik KA, Mirza MS, Hassan U, Mehnaz S, Rasul G, Haurat J, Bauy R, Normanel P (2002) The role of plant associated beneficial bacteria in rice-wheat cropping system. In: Kennedy IR, Chaudhry ATMA (eds) Biofertilisers in action. Rural Industries Research and Development Corporation, Canberra, pp 73–83Google Scholar
  93. Manjula K, Kishore GK, Podile AR (2004) Whole cells of Bacillus subtilis AF 1 proved effective than cell free and chitinase-based formulations in biological control of citrus fruit rot and groundnut rust. Can J Microbiol 50:737–744PubMedCrossRefGoogle Scholar
  94. Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fert Soils 30:433–439CrossRefGoogle Scholar
  95. Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops. Afr J Biotechnol 3(1):1–7Google Scholar
  96. Meyer SLF, Massoud SI, Chitwood DJ, Roberts DP (2000) Evaluation of Trichoderma virens and Burkholderia cepacia for antagonistic activity against root-knot nematode, Meloidogyne incognita. Nematology 2:871–879CrossRefGoogle Scholar
  97. Misko AL, Germida JJ (2002) Taxonomic and functional diversity of pseudomonads isolated from the roots of field-grown canola. FEMS Microbiol Ecol 42:399–407PubMedCrossRefGoogle Scholar
  98. Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296PubMedCrossRefGoogle Scholar
  99. Neilands JB, Nakamura K (1991) Detection, determination, isolation, characterization and regulation of microbial iron chelates. In: Winkelmann G (ed) CRC handbook of microbial iron chelates. CRC Press, LondonGoogle Scholar
  100. Nguyen TH, Deaker R, Kennedy IR, Roughly RJ (2003) The positive yield response of field-grown rice to introduction with a multistrain biofertiliser in the Hanoi area, Vietnam. Symbiosis 35:231–245Google Scholar
  101. Nielson P, Sorenson J (1997) Multi-target and medium independent fungal antagonism by hydrolytic enzymes in Paenibacillus polymyxa and Bacillus pumilus strains from barley rhizosphere. FEMS Microbiol Ecol 22:183–192CrossRefGoogle Scholar
  102. Nieto KF, Frankenberger WT Jr (1991) Influence of adenine, isopentyl alcohol and Azotobacter chroococcum on the vegetative growth of Zea mays. Plant Soil 135:213–221CrossRefGoogle Scholar
  103. O’Sullivan DJ, O’Gara F (1992) Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol Rev 56:662–676PubMedGoogle Scholar
  104. Okan Y, Kapulnik Y (1986) Development and function of Azospirillum inoculated roots. Plant Soil 90:3–16CrossRefGoogle Scholar
  105. Ordentlich A, Elad Y, Chet I (1988) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78:84–88Google Scholar
  106. Pal SS (1998) Interactions of an acid tolerant strain of phosphate solubilizing bacteria with a few acid tolerant crops. Plant Soil 198:169–177CrossRefGoogle Scholar
  107. Pal M, Karthikeyapandian V, Jain V, Srivastava AC, Raj A, Sengupta UK (2004) Biomass production and nutritional levels of berseem (Trifolium alexandrium) grown under elevated CO2. Agric Ecosyst Environ 101:31–38CrossRefGoogle Scholar
  108. Patten CL, Glick BR (2002) Role of Pseudomonas putida indole-acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801Google Scholar
  109. Paul EA, Clark FE (1996) Soil microbiology and biochemistry, 2nd edn. Academic, London, 340ppGoogle Scholar
  110. Paynel F, Murray PJ, Cliquet B (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229:235–243CrossRefGoogle Scholar
  111. Penrose DM, Glick BR (2001) Levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in exudates and extracts of canola seeds treated with plant growth promoting bacteria. Can J Microbiol 47:368–372PubMedCrossRefGoogle Scholar
  112. Peoples MB, Ladha JK, Herridge DF (1995) Enhancing legume N2 fixation through plant and soil management. Plant Soil 174:83–101CrossRefGoogle Scholar
  113. Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Leon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Sluis IV, Bakker PAHM, Van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression. Eur J Plant Pathol 107:51–61CrossRefGoogle Scholar
  114. Plessner O, Klapach T, Guerinot ML (1993) Siderophore utilization by Bradyrhizobium japonicum. Appl Environ Microbiol 59:1688–1690PubMedGoogle Scholar
  115. Podile AR, Kishore GK (2006) Plant growth promoting rhizobacteria. In: Gnanamanickam SS (ed) Plant associated bacteria. Springer, Amsterdam, pp 195–230CrossRefGoogle Scholar
  116. Ponmurugan P, Gopi C (2006) Distribution pattern and screening of phosphate solubilizing bacteria isolated from different food and forage crops. J Agron 5:600–604CrossRefGoogle Scholar
  117. Primrose SB (1979) Ethylene and agriculture: the role of the microbe. J Appl Bacteriol 46:1–25CrossRefGoogle Scholar
  118. Rao AV (2004) Microbial biotechnology for sustainable agricultural production in arid soils. In: Ray RC (ed) Soil microbial biotechnology for sustainable agricultural production. Oxford and IBH Publishing Co., New DelhiGoogle Scholar
  119. Rashid A (1996) Secondary and micronutrients. In: Rashid A, Memon KS (eds) Soil science. National Book Foundation, Islamabad, pp 341–385Google Scholar
  120. Reeves TG, Waddington SR, Ortiz-Monasterio I, Banziger M, Cassadey K (2002) Removing nutritional limits to maize and wheat production: a developing country perspective. In: Kennedy IR, Choudhury ATMA (eds) Biofertilizers in action. Rural Industries Research and Development Corporation, Canberra, pp 11–36Google Scholar
  121. Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M, Kersters K, DeLey J (1993) Azoarcus gen. Nov., nitrogen fixing proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth) and description of two species, Azoarcus indigens sp. Nov. and Azoarcus communis sp. Nov. Int J Syst Bacteriol 43:574–584CrossRefGoogle Scholar
  122. Reinhold-Hurek B, Egener T, Hurek T, Martin D, Sarkar A, Zhang L, Miche L (2002) Regulation of nitrogen fixation and assimilation of Azoarcus sp. BH72 new approaches to study biodiversity of grass endophytes. In: Vanderleyden J (ed) Proceedings of the ninth international symposium on nitrogen fixation with non-legumes. Katholique Universideit Leuven, Leuven, p 48Google Scholar
  123. Reis VM, Baldani JI, Baldani VLD, Döberener J (2000) Biological dinitrogen fixation in the graminae and palm trees. Crit Rev Plant Sci 19:227–247CrossRefGoogle Scholar
  124. Revillas JJ, Rodelas B, Pozo C, Martinez-Toledo MV, Gonzalez LJ (2000) Production of B-group vitamins by two Azotobacter strains with phenolic compounds as sole carbon source under diazotrophic and adiazotrophic conditions. J Appl Microbiol 89:486–493PubMedCrossRefGoogle Scholar
  125. Reyes E, Garcia-Castro I, Esquivelm F, Hornedo J, Cortes-Funes H, Solovera J, Alvarez-Mon M (1999) Granulocyte colony-stimulating factor (G-CSF) transiently suppresses mitogen-stimulated T-cell proliferative response. Br J Cancer 80(1/2):229–235PubMedCrossRefGoogle Scholar
  126. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  127. Riggs PG, Chelius MK, Iniguez AL, Kaeppler SM, Triplet EW (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:829–836Google Scholar
  128. Roos W (1984) Relationship between proton extrusion and fluxes of ammonium ions and organic acids in Penicillium cyrlopium. J Gen Microbiol 130:1007–1014Google Scholar
  129. Rosado AS, Seldin L (1993) Production of potentially novel anti-microbial substance by Bacillus polymyxa. World J Microbiol Biotechnol 9:521–528CrossRefGoogle Scholar
  130. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCrossRefGoogle Scholar
  131. Şahin F, Çakmakçi R, Kantar F (2004) Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant Soil 265:123–129CrossRefGoogle Scholar
  132. Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Suresh S, Samiyappan R (2008) Pseudomonas fluorescens enhances resistance and natural enemy population in rice plants against leaf folder pest. J Appl Entomol 132:469–479CrossRefGoogle Scholar
  133. Schalk IJ, Hennard C, Dugave C, Poole K, Abdallah MA, Pattus F (2001) Iron-free pyoverdin binds to its outer membrane receptor FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol Microbiol 39:351–360PubMedCrossRefGoogle Scholar
  134. Scharf PC (2001) Soil and plant tests to predict optimum nitrogen rates for corn. J Plant Nutr 24:805–826CrossRefGoogle Scholar
  135. Schippers B, Scheffer RJ, Lugtenberg JJ, Weisbek PJ (1995) Biocoating of seed with plant growth promoting rhizobacteria to improve plant establishment. Outlook Agric 24:179–185Google Scholar
  136. Shaharoona B, Arshad M, Zahir ZA, Khalid A (2006) Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol Biochem 38:2971–2975CrossRefGoogle Scholar
  137. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158:243–248PubMedCrossRefGoogle Scholar
  138. Sharma K, Dak G, Agrawal A, Bhatnagar M, Sharma R (2007) Effect of phosphate solubilizing bacteria on the germination of Cicer arietinum seeds and seedling growth. J Herb Med Toxicol 1:61–63Google Scholar
  139. Shiferaw B, Bantilan MCS, Serraj R (2004) Harnessing the potential of BNF for poor farmers: technological policy and institutional constraints and research need. In: Serraj R (ed) Symbiotic nitrogen fixation: prospects for enhanced application in tropical agriculture. Oxford and IBH publishing Co. Pvt. Ltd., New Delhi, p 3Google Scholar
  140. Shishido M, Breuil C, Christopher PC (1999) Endophytic colonization of spruce by plant growth promoting rhizobacteria. FEMS Microbiol Ecol 29:191–196CrossRefGoogle Scholar
  141. Singh S, Kapoor KK (1998) Inoculation with phosphate-solubilizing microorganisms and a vesicular-arbuscular mycorrhizal fungus improves dry matter yield and nutrient uptake by wheat grown in a sandy soil. Biol Fert Soils 28:139–144CrossRefGoogle Scholar
  142. Stajner D, Gasaić O, Matković B, Varga SZI (1995) Metolachlor effect on antioxidants enzyme activities and pigments content in seeds and young leaves of wheat (Triticum aestivum L.). Agr Med 125:267–273Google Scholar
  143. Stajner D, Kevreaan S, Gasaić O, Mimica-Dudić N, Zongli H (1997) Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol Plant 39:441–445Google Scholar
  144. Staunton S, Leprince F (1996) Effect of pH and some organic anions on the solubility of soil phosphate: implications for P bioavailability. Eur J Soil Sci 47:231–239CrossRefGoogle Scholar
  145. Stephen J, Jisha MS (2009) Buffering reduces phosphate solubilizing ability of selected strains of bacteria. World J Agric Sci 5:135–137Google Scholar
  146. Sudha SN, Jayakumar R, Sekar V (1999) Introduction and expression of the cry1Ac gene of Bacillus thuringiensis in a cereal-associated bacterium, Bacillus polymyxa. Curr Microbiol 38:163–167PubMedCrossRefGoogle Scholar
  147. Sundara B, Natarajan V, Hari K (2002) Influence of phosphorus solubilizing bacteria on the changes in soil available phosphorus and sugarcane yields. Field Crops Res 77:43–49CrossRefGoogle Scholar
  148. Tanaka H, Watanabe T (1995) Glucanases and chitinases of Bacillus circulans WL-12. J Ind Microbiol 114:478–483CrossRefGoogle Scholar
  149. Tang C, Rengel Z (2003) Role of plant cation/anion uptake ratio in soil acidification. In: Rengel Z (ed) Handbook of soil acidity. Marcel and Dekker, New York, pp 57–81Google Scholar
  150. Tao G, Tian S, Cai M, Xie G (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523CrossRefGoogle Scholar
  151. Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK, Nautiyal CS, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136–150Google Scholar
  152. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852CrossRefGoogle Scholar
  153. Tran Vân V, Berge O, Ke SN, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensis on early and late yield components in low fertility sulphate acid soils of Vietnam. Plant Soil 218:273–284CrossRefGoogle Scholar
  154. Urashima Y, Hori K (2003) Selection of PGPR which promotes the growth of spinach. Jpn J Soil Sci Plant Nutr 74:157–162Google Scholar
  155. Van Veen JA, Van Overbeek LS, Van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 16(2):121–135Google Scholar
  156. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
  157. Villegas J, Fortin JA (2002) Phosphorus solubilization and pH changes as a result of the interactions between soil bacteria and arbuscular mycorrhizal fungi on a medium containing NO3 as nitrogen source. Can J Bot 80:571–576CrossRefGoogle Scholar
  158. Walley FL, Germida JJ (1997) Response of spring wheat (Triticum aestivum) to interactions between Pseudomonas species and Glomus clarum NT4. Biol Fertil Soils 24:365–371CrossRefGoogle Scholar
  159. Walsh UF, Morrissey JP, O’Gara F (2001) Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr Opin Biotechnol 12:289–295Google Scholar
  160. Williams RL, Kennedy IR (2002) A model for testing the effectiveness of biofertiliser for Australian rice production. In: Choudhury ATMA, Kennedy IR (eds) Biofertilisers in action. Rural Industries Research and Development Corporation, Canberra, pp 112–114Google Scholar
  161. Yahya A, Azawi SKA (1998) Occurrence of phosphate solubilizing bacteria in some Iranian soils. Plant Soil 117:135–141CrossRefGoogle Scholar
  162. Yazdani M, Bahmanyar MA, Pirdashti H, Esmaili MA (2009) Effect of Phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of Corn (Zea mays L.). Proc World Acad Sci Eng Technol 37:90–92Google Scholar
  163. Zahir A, Muhammad A, Frankenberger WT Jr (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Advan Agron 81:97–168CrossRefGoogle Scholar
  164. Zaidi A (1999) Synergistic interactions of nitrogen fixing microorganisms with phosphate mobilizing microorganisms. Ph.D. thesis, Aligarh Muslim University, Aligarh, IndiaGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Rifat Hayat
    • 1
  • Iftikhar Ahmed
    • 2
  • Rizwan Ali Sheirdil
    • 1
  1. 1.Department of Soil Science and SWCPMAS Arid Agriculture UniversityRawalpindiPakistan
  2. 2.Plant Biotechnology ProgramNational Agricultural Research CentreIslamabadPakistan

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