Advances in ISSN: 2373-6402APAR

Plants & Agriculture Research
Review Article
Volume 4 Issue 6 - 2016
Plant Growth Promoting Rhizobacteria-an Efficient Tool for Agriculture Promotion
Deepmala Katiyar1*, A Hemantaranjan1 and Bharti Singh2
1Department of Plant Physiology, Institute of Agricultural Sciences, Banaras Hindu University, India
2Department of Microbiology, Institute of Medical Sciences, Banaras Hindu University, India
Received: September 25, 2016| Published: October 28, 2016
*Corresponding author: Deepmala Katiyar, Department of Plant physiology, Institute of Agricultural Sciences Banaras Hindu University, Uttar Pradesh, India, Tel: +054-267-029-390, +91945-226-7383; E mail:
Citation: Katiyar D, Hemantaranjan A, Singh B (2016) Plant Growth Promoting Rhizobacteria-an Efficient Tool for Agriculture Promotion. Adv Plants Agric Res 4(6): 00163. DOI: 10.15406/apar.2016.04.00163

Abstract

Current soil management strategies are mainly dependent on inorganic chemical-based fertilizers, which caused a serious threat to human health and environment. Plant growth-promoting rhizobacteria (PGPR) are naturally occurring soil bacteria that aggressively colonize plant roots and benefit plants by providing growth promotion. Inoculation of crop plants with certain strains of PGPR at an early stage of development improves biomass production through direct effects on root and shoots growth. The major groups of PGPR can be found along with the phyla actinobacteria, bacteroidetes, firmicutes, and proteobacteria. Inoculation of agricultural crops with PGPR may result in multiple effects on early-season plant growth, as seen in the enhancement of seedling germination, plant health, vigor, height, shoot weight, nutrient content of shoot tissues, early bloom, chlorophyll content, and increased nodulation in legumes. PGPRs are reported to influence the growth, yield, and nutrient uptake by an array of mechanisms. They help in increasing nitrogen fixation in legumes, help in promoting free-living nitrogen-fixing bacteria, increase supply of other nutrients, such as phosphorus, iron and produce plant hormones that enhance other beneficial bacteria or fungi. Now a day’s an increasing number of PGPR being commercialized for various crops. Subsequently, there has been much research interest in PGPRs. Several reviews have discussed specific aspects of growth promotion by PGPRs. Therefore, PGPRs can help to generate wealth cooperatively in local communities, reducing the need for more expensive manufactured products, such as nitrogenous fertilizers and use of PGPR in world has the potential to provide valuable insight.

Keywords: Plant growth promoting rhizobacteria (PGPR); Growth; Agriculture; Boifertilizers

Introduction

Conventional agriculture plays a significant role in meeting the food demands of a growing human population; this has also led to an increasing dependence on chemical fertilizers [1]. As agricultural production strengthened over the past few decades, farmers became more and more dependent on chemical fertilizers as a relatively reliable method of crop protection helping with economic stability of their manoeuvre. Chemical fertilizers are industrially manipulated substances composed of known quantities of nitrogen, phosphorus and potassium, and their exploitation causes air and ground water pollution by eutrophication of water bodies [2]. Nevertheless, increasing use of chemical inputs causes several negative effects, i.e., development of pathogen resistance to the applied agents and their non target environmental impacts [3,4]. An ample assortment of agriculturally important microorganisms have been taken use of crop health and production management, which comprise nitrogen fixers like Rhizobium, Bradyrhizobium, Sinorhizobium, Azotobacter, Azospirillum, phosphate solubilisers like Bacillus, Pseudomonas, Aspergillus, Enterobacter and Arbuscular mycorrhizae in agriculture. They are well known to increase plant growth, induce host plant resistance and crop yield [5]. The rhizosphere region has been distinct as the volume of soil directly influenced by the presence of living plant roots or soil compartment influenced by the root [6]. Rhizosphere supports large and active microbial population capable of exerting beneficial, neutral and detrimental effects on the plants. Various free-living soil bacteria that are capable of applying beneficial effects on plants in culture or in a protected environment via direct or indirect mechanisms [7,8]. The focus of this review is potential of PGPR which act as biofertilizers, either directly by helping to provide nutrient to the host plant, or indirectly by positively influencing root growth and morphology or by aiding other beneficial symbiotic relationships.

Effect of Chemical Fertilizers On Environment

Now a day an agricultural production can be increased efficiency by fertilization and it is only way for recovery of production. Non-organic synthetic fertilizers mainly contain phosphate, nitrate, ammonium and potassium salts. Fertilizer used to add nutrients to the soil to promote soil fertility and increase plant growth. They reduce the food value of plants. The nutrient reservoirs in the soil shrink when crops are removed from the field at harvest. This nutrient export creates a phosphorus deficit, necessitating regular phosphorus addition to replace the harvested phosphorus. This leads to the need of frequent application of chemical phosphate fertilizers, but its use on a regular basis has become a costly affair and also environmentally undesirable [9]. The excessive use of chemical fertilizers in plants not only affects the quality of food but also environment. Fertilizer industry is considered to be source of natural radionuclides and heavy metals as a potential source. It contains a large majority of the heavy metals like Cd, Pb, Hg and as [10,11] and some results in the accumulation of inorganic pollutants [12]. Plants absorb the fertilizers through the soil; they can enter the food chain. Thus, fertilization leads to water, soil and air pollutions. In recent years, fertilizer consumption increased continuously throughout the world, causes severe environmental problems as well as many diseases in human like Stomach cancer, goiter, and several vector borne diseases. In infants it is the reason of blue baby syndrome. It also leads to groundwater contamination [13]. There are also a number of fastidious diseases for which chemical solutions are few and ineffective [14]. Biological control is thus being considered as an alternative or a supplemental way of reducing the use of chemicals in agriculture [15].

Plant Growth-Promoting Bacteria (PGPR)

The narrow zone of soil directly surrounding the root system is referred to as rhizosphere [16], while the term ‘rhizobacteria’ implies a group of rhizosphere bacteria competent in colonizing the root environment [17]. About 2–5 % of the rhizosphere bacteria are PGPR [18]. The term PGPR was coined by Joe Kloepper in late 1970s and was defined by Kloepper and Schroth [19] as ‘‘the soil bacteria that colonize the roots of plants by following inoculation on to seed and that enhance plant growth’’. The rhizosphere, volume of soil surrounding roots and influenced chemically, physically and biologically by the plant root, is a highly favourable habitat for the proliferation of microorganisms and exerts a potential impact on plant health and soil fertility [20]. Root exudates rich in amino acids, monosaccharides and organic acids, serve as the primary source of nutrients, and support the dynamic growth and activities of various microorganisms within the vicinity of the roots [21]. On the basis of their location in rhizosphere PGPR can be classified as extracellular PGPR found in the rhizosphere, on the rhizoplane or in the spaces between the cells of the root cortex and intracellular PGPR which exist inside the root cells, generally in specialized nodular structures [22]. PGPR represent a wide variety of soil bacteria which grown in association with a host plant, result in stimulation of growth of their host. PGPR have the potential to contribute in the development of sustainable agricultural systems. In general, PGPR function in three different ways [23, 24]: synthesizing particular compounds for the plants [25,26] facilitating the uptake of certain nutrients from the soil [27] and preventing the plants diseases [28,29], (Figure 1).

Wide ranges of bacterial groups being considered as plant growth promoting rhizobacteria include Acinetobacter, Agrobacterium, Arthobacter, Azotobacter, Azospirillum, Burkholderia, Bradyrhizobium, Rhizobium, Serratia, Thiobacillus, Pseudomonads, and Bacilli in various plants [30,31], (Table 1).

Plant growth promoting rhizobacteria (PGPR)

Crops

Plant growth promoting traits

Literature cited in

Azospirillum sp.

Rice

Nitrogen fixation

[75]

Paenibacillus polymyxa

Wheat

Cytokinin

[112]

Pseudomonas rathonis

Wheat, Maize

Auxin production

[38]

Comamonas acidovorans

Lettuce

IAA production

[13]

Azoarcus sp.

Kallar grass

Nitrogen fixation

[58]

Kluyvera ascorbata
SUD 165

Canola, tomato

Siderophores,
IAA production

[117]

Azotobacter sp.

Sesbenia,

IAA production

[3]

Pseudomonas fluorescens

Soybean

Cytokinin

[33]

Azoarcus sp.

Rice

Nitrogen fixation

[39]

Enterobacter cloacae

Rice

IAA production

[79]

Pseudomonas sp.

Mungbean

IAA production

[2]

Alcaligenes sp.

Rape

ACC deaminase

[27]

Azoarcus sp.

Sorghum

Nitrogen fixation

[110]

Rhizobacterial isolates

Wheat, rice

Auxin production

[65]

Enterobacter sp.

Sugarcane

IAA production

[81]

Pseudomonas sp.

Wheat

IAA production

[94]

Azotobacter sp.

Maize

Nitrogen fixation

[90]

Pseudomonas fluorescens

Pine

Cytokinin

[18]

Rhizobium leguminosarum

Rice

IAA production

[31]

Pseudomonas sp. PS1

Greengram

Phosphate solubilization, Nitrogen fixation

[1]

Bacillus cereus RC 18,

Wheat

IAA production

[23]

Streptomyces, anthocysnicus, Pseudomonas aeruginosa, Pseudomonas pieketti

Rice

IAA production

[111]

Rhizobium leguminosarum

Rape & lettuce

Cytokinin

[85]

Bacillus licheniformis C08

spinach

IAA production

[111]

Rhizobium leguminosarum

Radish

IAA production

[6]

Azotobacter sp.

Wheat

Nitrogen fixation

[82]

Azotobacter sp.

Maize

IAA production

[117]

Mesorhizobium loti MP6, Pseudomonas fluorescens
ACC9, Alcaligenes sp. ZN4, Mycobacterium sp.

Brassica

Siderophore,
HCN production, IAA production

[27]

Pseudomonas tolaasii
ACC23,

Brassica

Siderophores,
IAA production

[35]

Bacillus polymyxa

Wheat

Nitrogen fixation

[89]

Bacillus pumilus

Rape

ACC deaminase

[16]

Pseudomonas fluorescens

Groundnut

Siderophores,
IAA production

[36]

Bacillus sp.

Alder

Gibberellin

[51]

Bacillus sp.

Rice

IAA production

[17]

Burkholderia sp.

Rice

Nitrogen fixation

[11]

Azospirillum lipoferum

Wheat

IAA production

[83]

Pseudomonas putida, Azospirilium, Azotobacter

Artichoke

Phosphate solublization

[57]

Gluconacetobacter diazotrophicus

Sorghum

Nitrogen fixation

[56]

Azospirillum brasilense

Wheat

IAA production

[62]

Enterobacter cloacae

Rape

ACC deaminase

[97]

Streptomyces acidiscabies
E13

Cowpea

Hydroxamate
siderophores

[37]

Gluconacetobacter diazotrophicus

Sugarcane

Nitrogen fixation

[20]

Pseudomonas sp.

Rape

ACC deaminase

[16]

Aeromonas veronii

Rice

IAA production

[79]

Bradyrhizobium sp.

Radish

IAA production

[6]

Pseudomonas cepacia

Soybean

ACC deaminase

[24]

Herbaspirillum sp.

Rice

Nitrogen fixation

[58]

Variovorax paradoxus

Rape

ACC deaminase

[21]

Herbaspirillum sp.

Sorghum

Nitrogen fixation

[58]

Agrobacterium sp.

Lettuce

IAA production

[13]

Pseudomonas putida

Mung bean

ACC deaminase

[78]

Herbaspirillum sp.

Sugarcane

Nitrogen fixation

[12]

Alcaligenes piechaudii

Lettuce

IAA production

[13]

Burkholderia verschuerenni Burkholderia sp.

Sugarcane

IAA production

[96]

Table 1: Plant growth promoting rhizobacteria (PGPR) for which evidence exists that their stimulation of plant growth promoting traits in numerous crops.

Figure 1: Major plant growth-promoting groups used in commercial bio-inocula for plant growth promotion.

The potential use of biofertilizers is now being seriously considered as a means to reduce the quantity of fertilizers required for crop production. This would help to minimize pollution and soil infertility, and above all reduce grower’s costs. PGPR have been reported to be present in high populations, in the rhizosphere and as endophytes of many crops. They include species of Enterobacter, Bacillus, Klebsiella, Herbaspirillum, Burkholderia, Azospirillum, and Gluconacetobacter [32]. The most common bacteria isolated from sugarcane tissues have been Gluconacetobacter diazotrophicus, Herbaspirillum rubrisubalbicans, and H. seropedicae [33], whereas Enterobacter cloacae, Erwinia herbicolla, K. pneumoniae, K. oxytoca, Azotobacter vinelandii, Paenibacillus polymyxa, and Azospirillum were found less often [33].

The growth promotion channel by these bacteria that enhances the plant growth was not fully known while in few ways it is understood [34]. The well known mechanism for the growth promotion is through producing various plant growth hormones that include Gibberellin and Indole-3-acetic acid (IAA) (Arshad and [35,23], solubilisation of insoluble phosphate [36] fixation of atmospheric nitrogen [37, 38] and hore synthesis [39], hydrogen cyanide production [40] and various antagonistic activity against the plant pathogens [41]. Therefore it is necessary to develop a rhizobacterial population that encompasses significant plant growth role for the improvement of agricultural practices and yield, thereby reducing the application of chemical biofertilizer and chemical pesticides, the present study was focused in the path to isolate an efficient PGPR strain from the rhizosphere of sugarcane plant and to assess the plant growth promoting activities.

Taxonomy of PGPR

Taxonomy is defined as the science dedicated to the study of relationships among organisms and has to do with their classification, nomenclature, and identification [42] The accurate comparison of organisms depends on a reliable taxonomic system. Even though many new characterization methods (including gene content, sequences of conserved macromolecules, gene order, dinucleotide relative abundance values and codon usage) have been developed over the last 30 years and used to study phylogenetic relationships between bacterial taxa [43].

PGPR Used As Biofertilizers

Biofertilizers, more commonly known as microbial inoculants, are artificially multiplied cultures of certain soil organisms that can improve soil fertility and crop productivity. Although the beneficial effects of legumes in improving soil fertility was known since ancient times and their role in biological nitrogen fixation was discovered more than a century ago, commercial exploitation of such biological processes is of recent interest and practice. The commercial history of biofertilizers began with the launch of ‘Nitragin’ by Nobbe and Hiltner, of Tharand, Germany, have invented certain new and useful improvements relating to the Inoculation of soil for the cultivation of leguminous plants and a laboratory culture of rhizobia in 1895, followed by the discovery of Azotobacter and then the blue green algae. Azospirillum and Vesicular- Arbuscular Micorrhizaeare fairly recent discoveries. In India the first study on legume rhizobium symbiosis was conducted by N.V. Joshi and the first commercial production started as early as 1956. However the Ministry of Agriculture under the ninth plan initiated the real effort to popularize and promote the input with the setting up of the National Project on Development and Use of Biofertilizers (NPDB). Commonly explored biofertilizers in India are mentioned below along with some salient features. Recently PGPR have attracted the attention of agriculturists as soil inoculums to improve plant growth and yield [44]. Significant increases in growth and yield of agronomically important crops in response to inoculation with PGPR have been repeatedly reported [45-55]. Studies have also shown that the growth-promoting ability of some bacteria may be highly specific to certain plant species, cultivar and genotype [56-58].  Plant growth-promoting rhizobacteria are the rhizospheric bacteria that can enhance plant growth by a wide variety of activities like:

Phosphate Solubilizing Bacteria

Phosphorus, both native in soil and applied in inorganic fertilizers becomes mostly unavailable to crops because of its low levels of mobility and solubility and its tendency to become fixed in soil. The phosphate sulubilizing (PSB) bacteria are life forms that can help in improving phosphate uptake of plants in different ways. The PSB also has the potential to make utilization of India’s abundant deposits of rock phosphates possible, much of which is not enriched. PSB are group of beneficial bacteria capable of hydrolyzing organic and inorganic phosphorus from insoluble compounds [59] Phosphate solubilization ability of the micro-organisms is considered to be one of the most important traits associated with plant phosphate nutrition [60]. It is generally accepted that mechanisms of the mineral phosphate solubilization by the PSB strains is associated with the release of low molecular weight organic acids, through which their hydroxyl and carboxyl groups chelate the cations bound to phosphate there by converting it into soluble forms [61].The PGPR occur in soil, usually their number are not high enough to compete with other microorganisms commonly established in the rhizosphere.

Thus the amount of P liberated by them is generally not sufficient for a substantial increase of in situ plant growth. Therefore inoculation of plants by a target microorganism at a much higher concentration than the normal found in soil is necessary to take advantage of the property of phosphate solubilization for plant yield enhancement [62]. Inoculation of PGPR in the soil is a promising technique because it can increase phosphorous availability [63] and improves the physio-chemical, biochemical and biological properties of soil [64]. So that use of PGPR in agriculture can not only compensate for higher cost of manufacturing fertilizers in industries but also mobilizes the fertilizers added to soil. In addition some PSB produce phosphatase like phytase that hydrolyse organic forms of phosphate compound efficiently.

Nitrogen Fixing Bacteria

About 78% of the earth atmosphere is made up of free nitrogen (N2) produced by biological and chemical processes within the biosphere and not combined with other elements. All plants need nitrogen for their growth. However plants cannot get the nitrogen they need from atmospheric supply. They can use only nitrogen that is available in compound form. Nitrogen occurs in the atmosphere as N2, a form that is not useable by plants. Nitrogen fixation is the first major mechanism for the enhancement of plant growth by Azospirillum [65]. Azospirillum species are aerobic heterotrophs that fix N2 under microaerobic conditions [66] and grow extensively in the rhizosphere of gramineous plants [67,68]. The Azospirillum–plant association leads to enhanced development and yield of different host plants [67]. This increase in yield is attributed mainly to an improvement in root development by an increase in water and mineral uptake, and to a lesser extent biological N2-fixation [68,69].

Siderophore Production

Iron is an essential nutrient for almost all forms of life. All microorganisms known so far, with the exception of certain lactobacilli, essentially require iron [70]. In the aerobic environment, iron occurs principally as Fe3+ and is likely to form insoluble hydroxides and oxyhydroxides, thus making it generally inaccessible to both plants and microorganisms. Despite being one of the most abundant elements in the earth’s crust, the bioavailability of iron in many environments such as the soil is limited by the very low solubility of the Fe3+ ion. It accumulates in commercial mineral phases such as iron oxides and hydroxides [71] therefore cannot be readily utilized by the organisms. Microbes release siderophores to scavenge iron from these mineral phases by formation of soluble Fe3+ complexes that can be taken up by the active transport mechanisms. Bacteria acquire iron by the secretion of low-molecular mass iron chelators referred to as siderophores which have high association constants for complexing iron. Most of siderophores are small, water soluble, high affinity iron chelating compounds amongst the strongest soluble Fe3+ binding agents known [72]. Thus, siderophores act as solubilizing agents for iron from minerals or organic compounds under conditions of iron limitation [73]. A great deal of evidence exists that a number of plant species can absorb bacterial Fe3+ siderophore complexes, and this process is vital in absorption of iron by plants [74].

Phytohormone Production

PGPRs produce plant hormones both in liquid cultures and natural condition. The major hormones produced are Indole acetic acid (IAA) [75]. It is reported that 80% of microorganisms isolated from the rhizosphere of various crops possess the ability to synthesize and release auxins as secondary metabolites [76]. IAA plays a very important role in rhizobacteria-plant interactions [77].  The IAA synthesized by PGPRs influenced the root hair development, respiration rate, metabolism and root proliferation which in turn resulted in better mineral uptake of the inoculated plants [78]. IAA formation via indole-3-pyruvic acid and indole-3-acetic aldehyde is found in a majority of bacteria like, Erwinia herbicola; saprophytic species of the genera Agrobacterium and Pseudomonas; certain representatives of Bradyrhizobium, Rhizobium, Azospirillum, Klebsiella, and Enterobacter. Most Rhizobium species have been shown to produce IAA [79].

 Nodule Forming Rhizobacteria

Biological N2 fixation represents the major source of N input in agricultural soils including those in arid regions. The major N2-fixing systems are the symbiotic systems, which can play a significant role in improving the fertility and productivity of low-N soils. The Rhizobium-legume symbioses have received most attention and have been examined extensively [80]. These Rhizobia (species of Rhizobium, Mesorhizobium, Bradyrhizobium, Azorhizobium, Allorhizobium and Sinorhizobium) inoculants are known for their ability to fix atmospheric nitrogen in symbiotic association with legume by responding chemotactically to flavonoid molecules released as signals by the legume host. These plant compounds induce the expression of nodulation (nod) genes in rhizobia, which in turn produce lipo-chitooligiosaccharide signals that trigger mitotic cell division in roots, leading to nodule formation [81-83]. The legume-Rhizobiumsymbiosis is a typical example of mutualism, but its evolutionary persistence is actually somewhat surprising. Because several unrelated strains infect each individual plant, any one strain could redirect resources from N2 fixation to its own reproduction without killing the host plant upon which they all depend [84-90]. It turns out that legume plants guide the evolution of rhizobia towards greater mutualism by reducing the oxygen supply to nodules that fix less N2 thereby reducing the frequency of cheaters in the next generation. Symbiotic N2-fixation has been studied widely and exploited as a means of increasing crop yields [91-94] but rhyzobium are however limited by their specificity and only certain legumes are benefited from this symbiosis [94-100].

Conclusions and future line Of work

This review has shown that there is huge potential for the use of PGPRs as biofertilizing agents for a wide variety of crop plants [97]. For this reason, there is an urgent need for research to clear definition of what bacterial traits are useful and necessary for different environmental conditions and plants [101-105]. They must be exploited to develop eco-friendly and safe replacement for chemical based fertilizers. Therefore, efficient PGPR strains can either be selected or improved [106,107]. The success of the science related to biofertilizers depends on inventions of innovative strategies related to the functions of PGPRs and their proper application to the field of agriculture [108-110]. The major challenge in this area of research lies in the fact that along with the identification of various strains of PGPRs and its properties it is essential to dissect the actual mechanism of functioning, synergistic effects of PGPRs for their efficacy toward exploitation in sustainable agriculture [111-115].  However, the triumph in developing PGPRs mediated tools is greatly dependent on the development of efficient and sensitive molecular genetics techniques like microarrays and effective culturing methodologies to provide a better insight of the structural and functional diversity of the rhizosphere [116-121]. Design of economically feasible large scale production methodologies and inoculation technologies are thus other critical requirements. So, deep rooted research in this area is highly needed. PGPRs are the potential tools for sustainable agriculture and trend for the future.

Acknowledgement

The Authors wish to thank University Grant Commission, New Delhi for financial support in form of Post Doctoral Fellowship (F.15-1/2012-13/PDFWM-2012-13-OB-UTT-17432). We are thankful to Department of Plant physiology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi for providing necessities of this work.

References

  1. Ahemad M, Khan MS (2012) Alleviation of fungicide-induced phytotoxicity in Greengram [Vigna radiata (L.) Wilczek] using fungicide-tolerant and plant growth promoting Pseudomonas strain. Saudi J Biol Sci 19(4): 451-459.
  2. Farah AHMAD, Iqbal Ahmad, Mohd Saghir KHAN (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and Flourescent pseudomonas in the presence and absence of tryptophan. Turk J Biol 29: 29-34.
  3. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92(5): 880-886.
  4. Alstrom S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soil 7: 232-238.
  5. Amara MAT, Dahdoh MSA (1997) Effect of inoculation with plant growth-promoting rhizobacteria (PGPR) on yield and uptake of nutrients by wheat grown on sandy soil. Egypt J Soil 37:467-484.
  6. Antoun H, Beauchamp CJ, Goussard N, Chabot R , Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant and Soil 204(1): 57-67.
  7. Antoun H, Prevost D (2005) Ecology of plant growth promoting rhizobacteria. In: Siddiqui ZA (Ed.) PGPR: biocontrol and biofertilization. Springer, Netherlands, p. 1–38.
  8. Araujo FF (2008) Inoculac¸a˜o de sementes com Bacillus subtilis, formulado com farinha de ostrase desenvolvimento de milho, soja e algoda˜o. Cieˆnc Agrotec 32:456–462.
  9. Arshad M Frankenberger Jr WT (1993) Microbial production of plant growth regulators. In: Blaine, F., Metting, Jr. (Eds.), Soil Microbial Ecology. Marcel and Dekker, Inc., New York, USA, pp. 307-347.
  10. Asghar HN, Zahir ZA, Arshad M, Khalig A (2002) Plant growth regulating substances in the rhizosphere: microbial production and functions. Advances in Agronomy 62:146-151.
  11. Baldani VLD, Baldani JI and Dobereiner J (2001) Inoculation of rice plants with the endophytic diazatrophs Herbaspirillum seropedicae and Burkholderia spp. Biology and Fertility of Soils 30(5): 485-491.
  12. Bar T, Okon Y (1993) Tryptophan conversion to indole-acetic acid via indole-3-acetamide in Azospirillum brasilense sp-7. Canadian Journal of Microbiology 39(1): 81-86.
  13. Barazani O, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? Journal of Chemical Ecology 25(10): 2397-2406.
  14. Barbieri P, Zanelli T, Galli E, Zanetti G (1986) Wheat inoculation with Azospirillum brasilense and some mutants altered in nitrogen fixation and indole-3 acetic acid production. FEMS Microbiology Letters 36(1): 87-90.
  15. Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnology Advances 16(4):729-770.
  16. Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, et al. (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47(7): 642-652.
  17. Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing Bacilli isolated from rice fields in South Brazil. Applied Soil Ecology 39(3): 311-320.
  18. Bent E, Tuzun S, Chanway CP and Enebak S (2001) Alterations in plant growth and in root hormone levels of lodgepole pines inoculated with rhizobacteria. Can J Microbiol 47(9): 793-800.
  19. Ahemad M, Khan MS (2011) Response of greengram [Vigna radiata (L.) Wilczek] grown in herbicide-amended soil to quizalafop- p-ethyl and clodinafop tolerant plant growth promoting Bradyrhizobium sp. (vigna) MRM6. J Agric Sci Technol 13:1209-1222.
  20. Boddey RM, Dobereiner J (1995) Nitrogen fixation associated with grasses and cereals: recent progress and perspectives for the future. Fertilizer Research 42(1): 241-250.
  21. Boddey RM, Polidoro JC, Resende AS, Alves BJR, Urquiaga S (2001) Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Australian Journal of Plant Physiology 28(9): 889-895.
  22. Boddey RM, Urquiaga S, Alves BJR, Reis V (2003) Endophytic nitrogen fixation in sugarcane: Present knowledge and future application. Plant Soil 252: 139-149.
  23. Çakmakçi R, Erat M, ErdoÄŸan 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: 288-295.
  24. Cattelan AJ, Hartel PG , Fuhrmann JJ (1999) Screening of plant growth promoting rhizobacteria to promote early soybean growth. J Soil Sci Soc Am 63(6): 1670-1680.
  25. Cattelan AJ, Hartel PG and Fuhrmann JJ (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63: 1670-1680.
  26. Çevre ve TC, Orman Bakanl O, Turkiye Çevre O Atlas ÇED O (2004) Planlama Genel Mudurlu ÷ü Çevre Envanteri Dairesi Baúkanl Õ ÷ Õ, Ankara.
  27. Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Brazilian Journal of Microbiology 124-130.
  28. Chen C, Bauske EM, Musson G, Rodriguez-Kaban˜a R, Kloepper JW (1994) Biological control of Fusarium on cotton by use of endophytic bacteria. Biological Control 5(1): 83-91.
  29. Chen YP, Rekha PD, Arun AB, Shen FT, Lai W, et al. (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Applied Soil Ecology 34(1): 33-41.
  30. Dakora FD (2003) Defining new roles for plant and rhizobia molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytologist 158(1): 39-49.
  31. Dazzo FB, Yanni YG, Rizk R, De Bruijn FJ, Rademaker J, Squartini, et al., (2000) Progress in multinational collaborative studies on the beneficial association between Rhizobium Ieguminosarum by trifolii and rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. IRR1, Los Banos, Philippines, pp. 167-189.
  32. De Freitas JR, Banerjee MR Germida JJ (1997)Phosphate Solubilizing rhizobacteria
  33. García de Salamone IE, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47(5): 404-411.
  34. De Weger LA, Van der Bij AJ, Dekkers LC, Simons M, Wijffelman CA, et al. (1995) Colonization of the rhizosphere of crop plants by plant-beneficial pseudomonas. FEMS Microbiology Ecology 17(4): 221-228.
  35. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium resistant rhizobacteria. Soil Biology Biochemistry 40(1):74-84.
  36. 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(4): 371-394.
  37. Dimkpa C, Aleš S, Dirk M, Georg B, Erika K (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microb 54(3): 163-172.
  38. Egamberdiyeva D (2005) Plant growth promoting rhizobacteria isolated from a calsisol in semi arid region of Uzbekistan: biochemical characterization and effectiveness. J Plant Nutr Soil Sci 168: 94-99.
  39. Egener T, Hurek T, Reinhold-Hurek B (1999) Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol Plant Microbe Interaction 12: 813-819.
  40. Enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soil 24: 358 - 364.
  41. Fallik E, Sarig S, Okon Y (1994) Morphology and physiology of plant roots associated with Azospirillum. In: Okon Y (Ed) Azospirillum-plant associations. CRC Press, Boca Raton, p. 77-84.
  42. FAO (2009) Resource S AT-Fertilizer. Food and Agriculture Organization of the United Nations.
  43. Fasim F, Ahmed N, Parson R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from air environment of a tannery. FEMS Microbiol Lett 213(1): 1-6.
  44. Figueiredo MVB, Burity HA, Martinez CR, Chanway CP (2008) Alleviation of water stress effects in common bean (Phaseolus vulgaris L.) by co-inoculation Paenibacillus x Rhizobium tropici. Applied Soil Ecoogyl 40:182-188.
  45. Gerhardson B (2002) Biological substitutes for pesticides.Trends Biotechnol 20(8): 338-343.
  46. Glick BR (1995) The enhancement of plant-growth by free-living bacteria. Canadian Journal of Microbiology 41(2):109-117.
  47. Glick BR, Patten CL, Holguin G, and Penrose DM (1999) Biochemical and Genetic Mechanisms Used by Plant Growth- Promoting Bacteria. Imperial College Press, London, UK.
  48. Govindarajan K, Kavitha K (2004) Studies on Azospirillum associated with rice varieties. In Biofertilizers Technology for Rice based Cropping System. Eds. S. Kannaiyan, K Kumar and K Govindarajan, Scientific Publishers, Jodhpur, India, pp. 221-224.
  49. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37(3): 395-412.
  50. Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, et al. (2004) Biocontrol of tomato wilt by plant growth promoting rhizobacteria. Biol Control 29(1): 66-72.
  51. Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, et al. (2001) The plant-growth promoting rhizobacteria Bacillus pumilusand Bacillus licheniformisproduce high amounts of physiologically active gibberellins. Physiol Plant 111: 206-211.
  52. Haas D, Blumer C, Keel C (2000) Bio control ability of fluorescent pseudomonas genetically dissected: importance of positive feedback regulation. Curr Opin Biotechnol 11(3): 290-297.
  53. Hiltner L (1904) UÈ ber neuere Erfahrungen und Probleme auf dem Gebiet der Bodenback teriologie und unter besonderer BeruÈcksichtigung der GruÈnduÈngung und Brache. ArbeitenDeutscher Landwirtschafts Gesellschaft 98: 59-78.
  54. 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(7): 1913-1923.
  55. Indiragandhi P, Anandham R, Madhaiyan M, Sa TM (2008) Characterization of plant growth-promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56(4): 327-333.
  56. Isopi R, Fabbri P, Del-Gallo M and Puppi G (1995) Dual inoculation of Sorghum bicolor(L.) Moench ssp. bicolor with vesicular arbuscular mycorrhizas and Acetobacter diazotrophicus. Symbiosis 18: 43–55.
  57. Jahanian A, Chaichi, MR, Rezaei K, Rezayazdi K, Khavazi K (2012) The effect of plant growth promoting rhizobacteria (PGPR) on germination and primary growth of artichoke (Cynara scolymus). Int J Agric Crop Sci 4: 923-929.
  58. James EK, Gyaneshwar P, Mathan N, Barraquio QL, Reddy PM, et al. (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15(9): 894-906.
  59. James EK, Olivares FL, Baldani JI, Dobereiner J (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in leaves of Sorghum bicolorL. Moench. Journal of Experimental Biology 48: 785-797.
  60. Jones D, Oburger E (2011) Solubilization of phosphorus by soil microorganisms. In: Bunemann, E., Oberson, A., Frossard, E. (Eds.), Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling, 26. Springer, pp. 169-198.
  61. Juanda JIH (2005) Screening of soil bacteria for Plant Growth Promoting Activities in Vitro. Journal of Agricultural Science 4(1): 27-31.
  62. Kaushik R, Saxena AK, Tilak KVBR (2000) Selection of Tn5::lacZ mutants isogenic to wild type Azospirillum brasilense strains capable of growing at sub-optimal temperature. World J Microbiol Biotechnol 16(6): 567-570.
  63. Kennedy IR, Choudhury AIMA, KecSkes ML (2004) Non-Symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Boilogy Biochemistry. 36(8):1229-1244.
  64. Kennedy IR, Tchan Y (1992) Biological nitrogen fixation in no leguminous field crops: recent advances. Plant Soil 141(1): 93-118.
  65. Khalid A, Arshad M, Zahir ZA (2001) Factor affecting auxin biosynthesis by wheat and rice rhizobacteria. Pak J Soil Sci 21:11–18.
  66. Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environmental Chemistry Letters 7(1): 1-19.
  67. Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In: Gilbert C (Ed) Proceedings 4th international conference on plant pathogenic bacteria, Tours, France, pp. 879-882.
  68. Kloepper JW, Schroth MN, Miller TD (1980) Effects of rhizosphere colonization by plant growth promoting rhizobacteria on potato plant development and yield. Ecology and Epidomology 70: 1078-1082.
  69. Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister, D.L., Cregan, P.B. (Eds.), The Rhizosphere and Plant Growth. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 315-326.
  70. Kumar RS, Ayyadurai N, Pandiaraja P, Reddy AV, Venkatesvarlu Y, et al. (2005) Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad spectrum antifungal activity and biofertilizing traits. J Appl Microbiol 98(1): 145-154.
  71. Kunc F, Macura J (1988) Mechanisms of adaptation and selection of microorganisms in the soil. In V Vancura & F Kunc (Eds.) Soil Microbial Associations, Elsevier Amsterdam.
  72. Lhuissier FGP, de Rujiter NCA, Sieberer BJ, Esseling JJ, Emons AMC (2001) Time of cell biological events evoked in root hairs by Rhizobiumnod factors: state of the art. Annals of Botany 87(3): 289-302.
  73. Lima E, Boddey RM, Dobereiner J (1987) Quantification of biological nitrogen fixation associated with sugarcane using 15N aided nitrogen balance. Soil Biol Biochem 19(2): 165-170.
  74. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Review Antonie Van Leeuwenhoek 86(1): 1-25.
  75. Malik K A, Bilal R, Mehnaz S, Rasul G, Mirza M S and Ali S (1997) Association of nitrogen-fixing, plant promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil 194(1): 37-44.
  76. Masalha J, Kosegarten H, Elmaci O, & Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biology and Fertility of Soils, 30(5): 433-439.
  77. Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops. African Journal of Biotechnology 3(1): 1-7.
  78. Mayak S, Tirosh T, Glick BR (1999) Effect of wild-type and mutant plant growth promoting rhizobacteria on the rooting of mung bean cuttings. J Plant Growth Regul 18(2): 49-53.
  79. Mehnaz S, Mirza MS, Haurat J, Bally R, Normand P, et al. (2001) Isolation and 16S rRNA sequence analysis of the beneficial bacteria from the rhizosphere of rice. Can J Microbiol 47(2): 110-117.
  80. Miller RL, Higgins VJ (1970) Association of cyanide with infection of birds foot trefoil by Stemphyliumloti. Phytopathology 60: 104-110.
  81. Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, et al. (2001) Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil 237(1): 47-54.
  82. Mrkovacki N, Milic V (2001) Use of Azotobacter chroococcumas potentially useful in agricultural application. Ann Microbiol 51: 145-158.
  83. Muratova A Yu, Turkovskaya OV, Antonyuk LP, Makarov OE, Pozdnyakova LI (2005) Oil-oxidizing potential of associative rhizobacteria of the genus Azospirillum. Microbiology 74(2): 210-215.
  84. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270(45): 26723-26726.
  85. Noel TC, Sheng C, Yost CK, Pharis RP and Hynes MF (1996) Rhizobium leguminosarumas a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42(3): 279-283.
  86. Oak A (1992) A re-evaluation of nitrogen assimilation in roots. Bioscience 42: 103-111.
  87. Okon Y, Itzigsohn R (1995) The development of Azospirillum as a commercial innoculant for improving crop yields. Biotechnol Adv 13(3):415-424.
  88. Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years world-wide field inoculation. Soil Biol Biochem 26(12): 1591-1601.
  89. Omar MNA, Mahrous NM, Hamouda AM (1996) Evaluating the efficiency of inoculating some diazatrophs on yield and protein content of 3 wheat cultivars under graded levels of nitrogen fertilization. Ann Agric Sci 41: 579-590.
  90. Pandey A, Sharma E and Palni L M S (1998) Influence of bacterial inoculation on maize in upland farming systems of the Sikkim Himalaya. Soil Biol Biochem 30: 379-384.
  91. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3- acetic acid. Can J Microbiol 42(3): 207-220.
  92. Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3): 142-149.
  93. Reddy MS, Kumar S, Khosla B (2002) Biosolubilization of poorly soluble rock phosphates by Aspergillus tubingensisand Aspergillus niger. Biores Technol 84(2): 187-189.
  94. Roesti D, Guar R, Johri BN, ImfeldG, Sharma S (2006) Plant growth stage, fertilizer management and bioinoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat field. Soil Biol Biochem 38:1111-1120.
  95. Roper MM, Ladha JK (1995) Biological N2-fixation by heterotrophic and phototrophic bacteria in association with straw. Plant Soil 174:211-224.
  96. Rosangela Naomi Inui - Kishi, Luciano Takeshi Kishi, Simone Cristina Picchi, José Carlos Barbosa, Maria Teresa Olivério Lemos, (2012) phosphorus solubilizing and iaa production activities in plant growth promoting rhizobacteria from brazilian soils under sugarcane cultivation Arpn journal of engineering and applied sciences 7(11).
  97. Saleh SS, Glick BR (2001) Involvement of gacS and rpoS in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can J Microbiol 47(8): 698-705.
  98. Santos VB, Araujo SF, Leite LF, Nunes LA, Melo JW (2012) Soil microbial biomass and organic matter fractions during transition from conventional to organic farming systems. Geoderma 170: 227-231.
  99. Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Suresh S, et al. (2008) Pseudomonas fluorescens enhances resistance and natural enemy population in rice plants against leaf folder pest. J Appl Entomol 132(6): 469-479.
  100. Savci S (2012) Investigation of Effect of Chemical Fertilizers on Environment. APCBEE Procedia 1: 287-292.
  101. Savci S (2012) An agricultural pollutant: Chemical fertilizer. International Journal of Environmental Sciences and Development 3: 77-80.
  102. Scher FM, Baker R (1982) Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressivenessto Fusarium wilt pathogens. Phytopathology 72: 15671573.
  103. Sevilla M, Burris RH, Gunapala N, Kennedy C (2001) Comparison of benefit to sugarcane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and Nif− mutant strains. Mol Plant Microbe Interact 14: 358-366.
  104. Shanahan P, O’Sullivan, Simpson DJ, Glennon P, O’Gara DF (1992) Isolation of 2,4-diacetylphlorogucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl Environ Microbiol 58(1): 353-358.
  105. Sharma PK, Kundu BS, Dogra RC (1993) Molecular mechanism of host specificity in legume-Rhizobiumsymbiosis. Biotechnol Adv 11(4):714-779.
  106. Silva VN, Silva LESF, Figueiredo MVB (2006) Atuac¸a˜o de rizo´bios com rizobacte´rias promotoras de crescimento em plantas na cultura do caupi (Vigna unguiculata L. Walp). Acta Sci Agron 28:407-412.
  107. Sonmez O, Kaplan M, Sonmez S (2007) An Investigation Of Seasonal Changes In Nitrate Contents Of Soils and Irrigation Waters In Greenhouses Located In Antalya-Demre Region. Asian Journal of Chemistry 19 (7): 5639-5646.
  108. Sorensen J (1997) The rhizosphere as a habitat for soil microorganisms. In J. D. van Elsas, JT Trevors , E MH Welington (Eds.). Modern Soil Ecology, New York: Marcel Dekker, Inc. pp. 21-46.
  109. Spaepen S, Vanderleyden J, Remans R (2007) Indole- 3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31(4): 425-448.
  110. Stein T, Hayen-Schneg N, Fendrik I (1997) Contribution of BNF by Azoarcussp. BH72 in Sorghum vulgare. Soil Biol Biochem 29: 969-971.
  111. Thakuria D, Taleekdar NC, Goswami C, Hazarika S, Boro RC, Khan MR (2004) Characterization and screening of bacteria from rhizosphere of rice grown in acidic soils of Assam. Curr Sci 86(7): 978-985.
  112. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biology and Biochemistry 31(13): 1847-1852.
  113. Vessey JK (2003) Plant growth-promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586.
  114. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1): 44-51.
  115. Welbaum GA, Sturz V, Dong Z and Nowak J (2004) Fertilizing soil microorganisms to improve productivity of agro ecosystems. Crit Rev Pl Sci 23:175-93.
  116. Youssef MMA, Eissa MFM (2014) Biofertilizers and their role in management of plant parasitic nematodes: A review. E3 Journal of Biotechnology and Pharmaceutical Research 5(1): 1-6.
  117. Zahir ZA, Abbas SA, Khalid M, Arshad M (2000) Substrate dependent microbially derived plant hormones for improving growth of maize seedlings. Pak J Biol Sci 3(2):289-291.
  118. Zahran HH (1999) Rhizobium-Legume Symbiosis and Nitrogen Fixation under Severe Conditions and in an Arid Climate. Microbiol Mol Biol Rev 63(4): 968-989.
  119. Zhang L, Fan J, Niu W, Jing Y (2011) Isolation of phosphate solubilizing fungus (Aspergillus niger) from Caragana rhizosphere and its potential for phosphate solubilization. Shengtai Xuebao/Acta Ecol Sin 31: 7571-7578.
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