promotion of plant growth by phytohormone

Chapter

PROMOTION OF PLANT GROWTH BY PHYTOHORMONE PRODUCING BACTERIA Md. Mohibul Alam Khan, Amena Khatun and Md. Tofazzal Islam Department of Biotechnology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh

ABSTRACT Bacteria from diverse taxonomic genera such as Bacillus, Pseudomonas, Azospirillum, Azotobacter, Acenetobacter, Rhizobium, Serratia, and Burkholderia are associated with plant either as epiphytes or endophytes. They play vital roles in growth and development of host plants through various mechanisms including fixation of atmospheric nitrogen, solubilization nutrients, protection of plants from biotic and abiotic stresses and production of hormonal substances. Production and secretion of the major phytohormones such as auxins, gibberellins, cytokinins, ethylene, etc. and their biosynthetic pathways in bacteria are well established. Application of phytohormone producing bacteria to plants as seed priming and/or root inoculation enhances growth and yield of crops. This chapter comprehensively reviews isolation, screening, molecular identification and characterization of phytohormone producing bacteria from plant and soils and discusses on potentials of these 

Corresponding author: Department of Biotechnology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur-1706, Bangladesh. E-mail: [email protected].

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Mohibul Alam Khan, Amena Khatun and Tofazzal Islam beneficial microorganisms as natural plant growth promoters in ecofriendly crop production. Biosynthetic pathways of phytohormones in the bacterial cells and their molecular cross-talks with host plants are also briefly discussed.

Keywords: plant growth promoting bacteria, plant-microbe interactions, auxin, gibberellins, Bacillus, rice rhizosphere

1. INTRODUCTION Chemical substances synthesized in plant cell that actively involve in a wide range of plant growth and developmental processes at a very low concentration are known as plant hormones or phytohormones [1]. Phytohormones also regulate the processes of reproduction, cell division or differentiation, development of seeds and leaves, germination of seeds, flowering, inhibition of stem elongation, and signaling and communication in plants. In fact, these substances are produced in specific tissues of plants and then transported to target tissues where they serve as signal molecules and stimulate specific physiological responses [2]. The concept of phytohormone as plant growth regulating substance was established in the late 19th century [3, 4]. Since then, ten different chemical groups of the basic phytohormones namely, auxins, cytokinins, gibberellins, ethylene, abscisic acid, polyamines, brassinosteroids, jasmonates, salicyclic acid and newly identified strigolactones have been reported [5]. Among them, five phytohormones, namely, auxins, gibberellins (GA), cytokinins, ethylene and absicic acid (ABA) are considered as the “Classical five” (Table 1) [6]. Since 1960, the world’s population has been doubled, which is projected to grow to 9.1 billion by 2050 [8]. To feed this fast growing population, annual cereal production will need to rise about 3 billion metric tons [9]. It has been estimated that the application of an additional 40 and 20 million metric tons of N and P fertilizers, respectively are needed to meet the increasing demand of food production by 2040 [10, 11]. This striking increase in the application of N and P fertilizers due to extensive agricultural practices has led to increase in the degradation of air and water quality, which is a threat to the Earth’s sustainability [12, 13]. Therefore, research focusing on improvement of plant growth and yield by reducing the use of chemical fertilizers to maintain sustainability and environmental quality has been given one of the prime preferences across the world.

Promotion of Plant Growth by Phytohormone Producing Bacteria

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Soil and plant-associated bacteria that colonize the plants following inoculation onto seed and enhance plant growth are called plant growth promoting bacteria (PGPB) [14, 15]. The PGPB exert beneficial effects on plant growth and development via direct and/or indirect mechanisms [16]. They can promote plant growth directly by synthesizing and secreting phytohormone or modulating the level of phytohormone in associated plant cell [16]. The PGPB that produce phytohormones are called “phytohormone producing bacteria” [17, 18]. Application of PGPB to plants as seed priming orinoculation results in enhanced plant growth and yield. For example, seed inoculation with indole-3acetic acid (IAA) producing Pseudomonas putida GR 12-2 stimulates the development of root system and promotes growth of the host plants [19]. Many soil bacteria produce either gibberellin or cytokinin or both [17, 20, 21] and promote plant growth [22, 23, 24]. A large body of literature indicated that soil and plant-associated bacteria produce various phytohormones and have potentials for the growth promotion of plants. However, the biosynthesis and regulation of these phytohormones in bacteria and mechanism of plant growth promotion by these bacterial metabolites are still poorly understood. In addition to phytohormone synthesis, many plant-associated bacteria are also known to promote plant growth by fixing atmospheric nitrogen [25, 26], solubilzing inorganic phosphate [27, 28], sequestering iron by siderophore production [29], and suppressing plant diseases by the production of antimicrobial substances [30, 31, 32, 33, 34] and/or induction of systemic resistance in the host plants [35]. Therefore, application of phytohormone producing bacteria to enhance growth and yield of crop plants in an eco-friendly manner has been considered as a promising alternative to expensive and environmentally harmful synthetic agrochemicals. Although several good reviews have recently been published on phosphate solubilizing [28], nitrogen fixing [26] and biological control [35] bacteria, there is no review has so far been published on phytohormone producing bacteria and their usage in low input sustainable agriculture. This chapter comprehensively reviews isolation and identification of plant-associated phytohormone producing bacteria and their application in the practical field as natural plant growth promoters. Biosynthetic pathways of major phytohormones in the bacterial cell and their modes of actions to host plants are also discussed. Please place Table 1 here.

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Mohibul Alam Khan, Amena Khatun and Tofazzal Islam

2. SOURCE OF ISOLATION, SCREENING, CHARACTERIZATION AND MOLECULAR IDENTIFICATION OF PHYTOHORMONE PRODUCING BACTERIA 2.1. Source of Isolation Soil is replete with microscopic life forms, where bacteria are by far the most common (ca. 95%) [16]. However, as plant root exudes numerous organic substances (photosynthates) including sugars, amino acids, organic acids, and other small molecules, bacterial population in the rhizosphere are usually much greater than in soils without plant [36, 37]. The narrow zone of soil specifically influenced by the plant root system and plant produced material is referred to as rhizosphere [38, 39]. A large number of indole-3acetic-acid (IAA) producing bacteria have been isolated from the rhizosphere of rice [40, 41], wheat [42], sugarcane and ground nut [43], maize and broad bean [44], black gram [45], sweet potato [46], chickpea [47], banana and cotton [48], tomato and carrot [49]; and rhizoplane of maize, wheat and rice [50], and Spartina and Juncus [51] (Table 2). In addition, IAA producing epiphytic and endophytic bacteria has been found in roots, leaves and stems of soybeans [52]. Not only IAA, gibberellic acid (GA) and cytokinin producing bacteria from plants and soils have also been isolated and identified [53, 54, 55] (Table 2-4). For example, both IAA and gibberellic acid (GA) producing bacteria have been isolated from the rhizosphere and non-rhizosphere of salt-affected soils [54] (Table 3). Cytokinin producing bacteria have also been isolated from surface sterilized leaves of Tabernaemontana divaricata [55] and Gynura procumbens (Lour.) Merr [53] (Table 4). Table 2, 3 and 4 should be moved here.

2.2. Screening 2.2.1. Auxin Colorimetric technique is typically employed to screen for IAA producing bacteria [56, 57, 58]. This method was first described by Mitchell and Brunstetter (1939) [59] and later improved by Tang and Bonner (1947) [60] and by Gordon and Weber (1951) [61]. With slight modifications, colorimetric


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method has long been used by many researchers for the isolation of IAA producing bacteria [40, 41, 44, 49, 56]. It is a very useful tool for screening of IAA producing bacteria, but it requires cell free supernatants or purified extracts and the use of sophisticated instruments (Figure 1) [62]. In contrast, this method is time consuming and laborious [57, 58]. Bric et al. (1991) [57] and Shrivastava and Kumar (2011) [58] proposed alternative methods for the faster screening of IAA producing bacteria.

2.2.2. Gibberellins Methodical advancement for quantitative estimation of giberellic acids (GAs) produced by soil or plant-associated bacteria is scarce. A qualitative method for screening GA producing bacteria was described by Brown and Burlingham (1968) [63]. Further work is warranted to develop a convenient and quantitative method for the estimation of GAs produced by bacteria. 2.2.3. Cytokinins To isolate and screen cytokinin producing bacteria, the cucumber greening bioassay, described by Fletcher and McCuliagh (1971) [64], has widely been used as a convenient and sensitive technique [53, 55, 65].

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Figure 1. Supernatant of culture broth of a rhizobacterium Serratia marcescens (BTLbbc-07) showed pink color (right hand side one) after addition of Salkowski reagent indicating the presence of IAA (16.4 µg/ml) produced by BTLbbc-07 [62].

This method was later modified and substantially improved by Fletcher et al. (1982) [66]. The principle of this assay is based on ability of a bacterium produced cytokinin to stimulate greening in etiolated cucumber cotyledons [66, 67]. A more convenient quantitative method for estimation of cytokinin produced by bacteria is also warranted.

2.3. Characterization and Molecular Identification Generally, polyphasic taxonomical studies such as phenotypic, genetic, and phylogenetic information have been used in bacterial diversity studies [68]. Phenotype information includes morphological, physiological, and biochemical features of the bacteria [69]. Gram staining, motility, fluorescence on King’s B (KB) medium, oxidase and catalase reactions, production of arginine dihydrolase, levan formation, gelatin liquefaction, nitrate reduction, growth at 4°C and 42°C, and carbon utilization profile are generally used to determine the phenotypic variations among the bacteria [28, 70]. In fact, phenotypic features are not enough to precisely identify a bacterial isolate [28]. Therefore, molecular techniques such as gene sequencing are used to identify newly isolated environmental bacteria [28, 71]. Although, all three kinds of rRNA molecules, i.e., 5S, 16S and 23S and spacers between these can be used for phylogenetic analyses, however, 16S rRNA gene is the most commonly used as phylogenetic marker in the ecology of PGPB [72, 73, 74]. Based on the 16S rRNA gene sequencing data, a large number of phytohormone producing bacteria such as Streptomyces sp. ASU1 4 [44], Klebsiella SN 1.1 [41], Promicromonospora sp. SE188 [75], Alcaligenes faecalis [55], and several strains belonging to the genus Pseudomonas, Ralstonia, Enterobacter, Pantoea and Acinetobacter [52] have been identified. Polyphasic taxonomical analyses including gene sequencing have been found useful for identification of new PGPB species, such as Pseudomonas rhizospherae [76], P. lutea [77], and Microbacterium ulmi [78]. However, sequences of other highly conserved housekeeping or protein encoding genes, such as rpoB, gyrB, and recA, have also great potentials for taxonomic analysis of bacteria at the species level. For example, Wang et al. (2007) [79] examined gyrB sequence comparisons in the studies of the Bacillus subtilis group, while Cerritos et al.


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(2008) [80] examined recA sequence comparisons in the work that led to the proposal of a new Bacillus species. Other molecular techniques including direct electrophoresis of amplified fragments by PCR, such as RAPD and BOX PCR are found effective in biodiversity studies of the bacteria [70, 73], but at an intra-specific level [81].

3. EFFECTS OF PHYTOHORMONE PRODUCING BACTERIA ON PLANT A wide range of phytohormone producing bacteria have been reported with profound effects on nutrient uptake, seed germination, growth and development, yield, quality and plant disease reduction in their host plants [82, 83, 84, 85]. They play a pivotal role in cycling of nutrients within the soil and increasing the supply of nutrients such as nitrogen, phosphorus, sulphur, potassium, iron and copper in available forms to the plants.

3.1. Seed Germination The vital phytohormone cytokinin promotes germination of plant seeds by antagonizing ABA-mediated inhibitory effect. Conversely another phytohormone abscisic acid (ABA) plays an important role in plants by inhibiting seed germination and post-germinative growth [86]. Seed bacterization with phytohormone producing bacteria enhances seed germination. For example, Azospirillum brasilense strain Az39 and Brayrhizobium japonicum strain E109 produce appreciable amounts of indole3-acetic acid (IAA), gibberellic acid (GA3) and zeatin (Z). Cassán et al. (2011) [87] have shown that such compounds are responsible for early growth promotion in inoculated corn (Zea mays L.) and soybean (Glycine max L.) seedlings. When seeds were inoculated with Az39 and E109 and kept in a chamber at 20-30°C under a controlled photoperiod to evaluate seed germination, Az39 and E109 showed the capacity to promote seed germination singly or in combination. Both strains were able to excrete sufficient amount of IAA, GA3 and Z into the culture medium to enhance morphological and physiological changes in the seed tissues [87].

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Phytohormone producing Bacillus megaterium var. phosphaticum and Azotobacter chroococcum treated maize seeds showed more than 20% increased seed germination over control [88].

Figure 2. Photographs showing the effrects of Serratia marcescens (BTLbbc-07) (right) on growth promotion of Cucumis sativus over control (left) [62]. Seed bacterization resulted in higher shoot: root growth and shoot biomass of cucumber plants. Moreover, S. marcescens (BTLbbc-07) showed significantly higher increase in shoot dry weight and root dry weight (right) over untreated control (left) [62].

Cytokinin have since been implicated in a broad range of developmental processes including seed germination [1] by influencing cell division in the embryonic as well as mature plants by altering the size and activity of meristems [89, 90]. The IAA producing bacterium, Serratia marcescens (BTLbbc-07) enhanced significant growth promotion in cucumber seedlings [62].

3.2. Seedling Growth and Development Enhancement of phytohormone producing bacteria on seedling growth and development has been reported by a number of researchers [91]. It has been shown that bacterial phytohormones are involved in the interactions between plant and endophytic or free-living plant growth promoting rhizobacteria. IAA producing Bacillus megaterium from tea rhizosphere enhances plant growth promotion [92]. The cytokinin receptors of Bacillus megaterium play a complimentary role in plant growth promotion [93]. In drought stressed plants,


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inoculation with bacteria producing cytokinin has been shown to stimulate shoot growth and reduce root/shoot ratio [94]. A great potentiality of gibberellins (GAs) producing bacteria is to play a role in abiotic stresses particularly drought and salinity [75]. The ubiquitous phytohormone, gibberellins (GAs) can elicit various metabolic function required during each plant growth stages such as seed germination, stem elongation, sex expression, flowering, formation of fruits, and senescence [95]. However, alteration of ethylene levels with beneficial effects on plant’s root and shoot biomass has been reported [96, 97]. Furthermore, auxin producing Azospirillum stimulates root proliferation of plants [98]. Rice seeds inoculated with Rhizobium leguminosarum and Azotobacter sp. produced indole-3-acetic acid, which had significant growth promoting effects on rice and maize seedlings [99].

3.3. Nutrient Uptake by Plants Phytohormone producing bacteria belonging to the genera Azotobacter, Azospirillum, Pseudomonas, Acetobacter, Herbaspirillum, Burkholderia and Bacillus are involved in nutrient uptake by plant [91]. As a result of coevolution, rhizospheric bacterial communities have efficient systems for uptake and catabolism of organic compounds present in root exudates. For example, Azospirillum inoculation increased plant dry weight and nitrogen assimilation by 25% [100]. Çakmakci et al. (2007a) [101] showed that the most important phytohormone ‘auxin’ producing Bacillus licheniformis RC02, Rhodobacter capsulatus RC04, Paenibacillus polymyxa RC05, Pseudomonas putida RC06, and Bacillus OSU-142 strains fixed N2 and significantly increased the growth of barley. These results suggest that seed inoculation of barley with phytohormone producing bacteria can increase root and shoot weight by 18-32% and 29-54% compared to untreated control. Additionally, inoculation of phytohormone producing bacteria significantly increased uptake of N, Fe, Mn, and Zn by barley. Moreover, IAA producing bacteria Pseudomonas aeruginosa promote nitrogen and phosphorus uptake by chickpea [102].

3.4. Suppression of Disease

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Auxin and other phytohormone producing bacteria have immediate effects on phytopathogens [103] as well as impact on other physiological processes of plants. For example, Azospirillum brasilense produces phenylacetic acid, related to auxins, which are able to antagonize plant pathogens [104]. Bradyrhizobium japonicum associated with soybean roots produces rhizobitoxine, which give protection against the pathogenic fungus Macrophomina phaseolina [105]. Various plant growth promoting bacteria produce the enzyme 1-aminocyclopropane-1-carboxylate deaminase (ACCD), which can cleave the immediate precursor ACC of phytohormone ethylene in plants, to -ketobutyrate and ammonia. It was observed that the presence of ACCD was inhibitory to tumor development in both tomato and castor bean plants [106]. Additionally, phytohormone producing bacteria can indirectly influence a host’s defensive status by two ways, altering the expression of plant defense pathways and by increasing host vigor [107].

3.5. Yield and Quality of Produce Noticeable increase in crop yield was observed due to the production of phytohormones such as zeatin, gibberellic acid and abscisic acid by the bacterial inoculant such as Bacillus subtilis [108]. These bacterial phytohormones transport into the shoot through the xylem. Intensified and prolonged synthesis of these phytohormones delay senescence and improve yield of crop plant. For example, B. subtilis isolate increased yield of plants in addition to inducing resistance to the biotrophic fungal phytopathogens [109]. Pseudomonas fluorescens and P. putida are two important species of the PGPR, which produce auxin and promote the yield of lettuce, tomato and pepper plants [110]. The application of B. subtilis leads to stronger root growth and increases synthesis of plant cytokinins, which cause delayed senescence and higher yields in lettuce, tomato and pepper production [110]. B. polymyxa had positive effect on enzymatic activities of cucumber plants and had significant effect on increase in cucumber yield up to 25% compared to control [111, 112]. Gibberellins (GAs) producing bacteria regulate levels of plant hormone in different ways: by direct synthesis of GAs itself, de-conjugation of glucosyl gibberellins, and changing inactive state of gibberellins into active GAs which promotes better crop yield [112, 113].


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4. BIOSYNTHESIS OF PHYTOHORMONES IN BACTERIA The functions of phytohormone biosynthesis in bacteria is a subject of intense investigation but the detail pathways of biosynthesis are not yet completely elucidated. Auxin biosynthesis by Pseudomonas, Agrobacterium, Rhizobium, Bradyrhizobium, and Azospirillum, has been investigated extensively. In these bacteria, several physiological effects have been correlated to their biosynthesis of phytohormones.

4.1. Biosynthesis of Auxin Many plant-associated bacteria synthesize auxins, more commonly indole3-acetic acid (IAA), in order to perturb host physiological processes for their own benefit. Although bacteria can synthesize IAA through six different pathways namely, indole-3-acetamide (IAM), indole-3-pyruvic acid (IPA), tryptamine (TAM), indole-3-acetonitrile (IAN), tryptophan side-chain oxidase (TSO) and tryptophan independent pathways, a high degree of similarity between biosynthesis of IAA in plants and bacteria has been reported (Figure 3) [84, 134]. An amino acid, tryptophan, is identified as the main precursor for IAA biosynthesis in bacteria. Although the general mechanism of auxin biosynthesis is mainly concentrated on the tryptophan-independent pathways, five of the six pathways for auxin synthesis in bacteria are dependent on tryptophan as the main precursor [84]. The indole-3-acetamide (IAM) pathway has been reported in many bacteria such as Agrobacterium tumefaciens, Pseudomonas syringae, and P. savastanoi [82, 84, 135, 136]. In the IAM pathway, there are two enzymes involved namely, tryptophan monoxygenase (IaaM) and indole-3-acetamide hydrolase (IaaH). The IaaM oxidizes tryptophan to indole-3-acetamide after which IaaH converts indole-3-acetamide to IAA by hydroxylation. Interestingly, these IaaM and IaaH enzymes are only found in microorganisms [7, 137]. The indole-3-pyruvic acid (IPA) is one of the major tryptophan-dependent IAA synthetic pathways in plant growth-promoting bacteria Azospirillum sp., Agrobacterium rhizogenes and Pseudomonas savastanoi [82]. Tryptophan transaminase deaminates tryptophan to produce IPA. The IPA is then decarboxylated by the action of IPA decarboxylase to produce indole-3acetaldehyde (IALd). IALd is then oxidized to IAA by IAld dehydrogenase [7,

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137]. The IPA pathway has been reported in many bacteria like Erwinia herbicola, Rhodococcus fascians, etc. [138, 139, 140, 141, 142]. The tryptamine (TAM) pathway is almost similar to the IPA pathway; the only difference between these two pathways is the order of the deamination and decarboxylation reactions [134].

Table 1. Structural formulae and major function of phytohormones in plants [7]

Table 2. IAA producing bacteria and their effects on growth and yield of crop plants

Table 3. Effect of gibberellin producing bacteria on growth and yield of crop plants

Table 4. Effect of cytokinins and other phytohormone producing bacteria on plants

IAAld, indole-3-acetaldehyde; IAM, indole-3-acetamide; IPDC, indole-3-pyruvate decarboxylase; Trp, tryptophan. Figure 3. Overview of the different pathways to synthesize IAA in bacteria [84]. The intermediate referring to the name of the pathway or the pathway itself is underlined.

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The indole-3-acetonitrile (IAN) pathway converts tryptophan to indole-3acetaldoxime which is then converted to indole-3-acetonitrile. The enzyme, nitrilase, can convert indole-3-acetonitrile (IAN) to IAA. Some bacteria e.g., Agrobacterium and Rhizobium use this pathway to synthesize IAA [143, 144]. Tryptophan side-chain oxidase (TSO) activity has been demonstrated in Pseudomonas fluorescens CHA0. In this pathway, tryptophan is directly converted to IAAld bypassing IPyA, which can be oxidized to IAA [145]. However, some bacteria can synthesize IAA through more than one pathway. For example, in Pantoea agglomerans, genes for the IAM as well as for the IPyA pathway have been identified [142]. As tryptophan is the major precursor of tryptophan dependent biosynthetic pathways of IAA synthesis, it plays a key role in modulating the level of IAA biosynthesis [146]. Increased IAA production with tryptophan supplementation in culture media by most of the rhizobacteria has been reported [147]. Interestingly, tryptophan stimulates IAA synthesis while, anthranilate, a precursor for tryptophan, reduces the synthesis of IAA. By this mechanism, IAA biosynthesis is well-regulated in bacteria [84]. In addition, environmental stress factors such as, acidic pH, osmotic and matrix stress, and carbon limitation was found to modulate the IAA biosynthesis in different bacteria [84]. Among genetic factors, both the location of auxin biosynthesis genes in the bacterial genome (either plasmid or chromosomal) and the mode of expression (constitutive vs. induced) have been found to affect the level of IAA production.

4.2. Biosynthesis of Gibberellins The ability of bacteria to synthesize gibberellin-like substances was first reported in Azospirillum brasilense [132] and Rhizobium [148]. Later, it has been reported in different bacterial genera including, Azotobacter, Arthrobacter, Azospirillum, Pseudomonas, Bacillus, Acinetobacter, Flavobacterium, Micrococcus, Agrobacterium, Clostridium, Rhizobium, Burkholderia, Bradyrhizobium and Xanthomonas [18, 22, 112, 149, 150, 151, 152, 153, 154, 155, 156, 156]. While the biosynthetic pathways leading to gibberellin synthesis in both plants [157] and fungi [158] are already known, the detail mechanism of gibberellin biosynthesis in bacteria is yet to be fully understood [159, 160]. However, the existence of two branches for the biosynthetic pathway in Azospirillum i.e., early 13-hydroxylation involving the metabolism of GA19 (and its metabolite, GA20) to GA1, and an early nonhydroxylation branch where GA9 is (presumably) the precursor of GA3


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has been reported [161]. This concept is also reinforced by the effect of blue light on A. lipoferum cultures, i.e., a 2- to 3- fold increase in the amount of GA3, relative to GA1 [161]. In addition, effect of other environmental factors in gibberellins biosynthesis, such as N supply [162], O2 availability and osmotic potential [163], and high concentrations of NH4Cl [162] have been reported. Gibberellins are formed from geranylgeranyl diphosphate (GGPP) [164]; however, initial steps of the gibberellins biosynthetic pathway in bacteria may be regulated by membrane related cytochrome P450 monooxygenases, and the late hydroxylative steps by soluble 2-oxoglutarate-dependent dioxygenases [154]. The putative pathway for gibberellins biosynthesis in Azospirillum sp. has been discussed in details by Bottini et al. in 2004 [154]. Furthermore, in Bradyrhizobium japonicum, an operon consisting of genes which encoded a ferredoxin, a short chain alcohol dehydrogenase, three P450s, a GGPP synthase, and two (di)terepene synthases has been suggested to be associated in gibberellins biosynthesis [165].

4.3. Biosynthesis of Cytokinins Many bacterial genera including Azotobacter, Azospirillum, Rhizobium, Bacillus, and Pseudomonas have been reported to produce cytokinins [17, 20, 21, 166]. The condensation of AMP and dimethylallyl pyrophosphate (DMAPP) to the active cytokinin isopentenyladenosine-5ʹ-monophosphate (iPMP), catalyzed by a DMAPP: AMP transferase is considered as the major pathway for cytokinin biosynthesis in bacteria [133]. The principal cytokinins isopentenyl adenine (iP), isopentenyl adenosine (iPA), or their phosphorylated derivatives are hydroxylated to form the highly biologically active t-zeatin derivatives [167, 168, 169]. The ipt gene which encodes the key enzyme isopentenyl transferase, responsible for the biosynthesis of cytokinins, catalyzes the transfer of the isopentenyl moiety from DMAPP. It was initially characterized in Agrobacterium tumefaciens [170] and subsequently found in methylotrophic and methanotrophic bacteria [171, 172]. However, nopaline-producing A. tumefaciens strains posses another gene for DMAPP: AMP isopentenyltransferase, tzs gene, which is responsible for the high level of cytokinin production by these strains [173]. Genes that resemble ipt and tzs are also found in Pseudomonas syringae pv. “Savastanoi” [174], P. solanacearum [175], Erwinia herbicola [134] and Rhodococcus fascians [176].

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On the contrary, cytokinins may also be derived indirectly from tRNA in Agrobacterium tumefaciens in which a DMAPP: tRNA transferase (miaA) was characterized by Gray et al. (1992) [177].

5. MECHANISM OF PLANT GROWTH AND DEVELOPMENT BY PHYTOHORMONE PRODUCING BACTERIA A wide range of bacterial species possess the ability to produce the phytohormone through pathogenesis to phytostimulations. Phytohormones regulate throughout the plant cell cycle, cell division, cell elongation and differentiation to root initiation, apical dominance, trophistic responses, flowering, fruit ripening and senescence processes. For example, IAA regulates many aspects of plant growth and development. Some phytohormone producing bacteria can also produce secondary metabolites that induce phytohormone production in plants. They also play a key role in a plant's response to biotic and abiotic stresses. Although mechanisms are not yet elucidated in detail, the plant-associated bacteria have the potential to manipulate plant physiology and steer it toward outcomes that favor their own survival. It is known that IAA acts as a bacterial signal beside the manipulation of host physiology [84]. Quorum sensing (QS) and autoactivation mechanisms are involved with IAA synthesis in plant growth-promoting Azospirillum species. Some other epiphytic plant-associated bacteria can actively destroy IAA which is quite common on plant surfaces [178]. These bacteria are able to degrade IAA partially and able to disrupt IAAbased signaling equally. After that those degradation products of IAA are turned into signaling molecules [179]. Some, like isatin has a demonstrated signaling function in bacterial biofilm formation, and salicylate is a plant hormone involved in the plant response to pathogens. Both isatin and salicylate can be derived from the degradation of IAA. Microbial IAA as a manipulative and/or signaling molecule has direct and indirect impact of microbial interactions on plant health. IAA producing bacteria have the potential to interfere with any of these processes by input of IAA into the plant’s auxin pool [180] which plays a key role in the regulation of plant growth and development.


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Figure 4. Relationships among bacterial phytohormone mediated mechanisms, plant functional traits, plant bacterial phytohormone (e.g., auxins) production altering the root: shoot ration and hence biomass, which then changes both plant demography and ecosystem service productivity. Finally, phytohormones such as auxins, gibberellins, cytokinins can influence multiple functional traits.

Phytohormone producing plant-associated bacteria could be important components of the proximate mechanisms underlying plant functional traits (Figure 4). Nearly 50% of plant functional traits are influenced by bacterial mediation. These include most leaf traits and all root traits [181, 182]. The phytohormone producing bacteria can alter plant physiological pathways and mediate plant functional traits by two distinct ways – a) by providing novel biochemical capabilities and b) by altering existing plant pathways [182]. The phytohormone auxin influences some aspects of plant architecture. Azospirillum producing hormone stimulates plant’s physiology which causes root proliferation [98]. Quorum-sensing signals, acyl homoserine lactones (AHLs) can modify root development in Arabidopsis [93] through primary root growth, lateral root formation, and root hair development. Many plantassociated rhizobacteria found on root surfaces, can alter ethylene levels with beneficial effects on above-ground biomass [e.g., 96]. Moreover, rhizobacteria Phyllobacterium provides improved root architechture in the presence of nitrate. It is well known that bacterial IAA can stimulate ethylene production through the activation of the 1-aminocyclopropane 1-carboxylate synthase (ACS) [183]. Moreover, ethylene mediates plant autoregulation of nodulation in actinorhizal plants [184]. The bacterial ethylene in legumes such as alfalfa [186] also caused nodulation in roots, which helps to uptake nitrogen. Rhizoactinomycete strains improve alfalfa plant’s growth and development through increasing of shoot weight and dry biomass, root dry weight and nodule number [186, 187]. It has been reported that bacterial elicitor like Pseudomonas fluorescens treatments had improved phytohormonal characters of maize (Zea mays L.) under water deficit [188].

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Thus phytohormone producing bacteria can enhance phytohormones content of plants and regulate the growth and development throughout the vegetative and reproductive stage.

6. BIOFERTILIZERS BASED ON HORMONE PRODUCING BACTERIA Biofertilizer can be defined as a substance which contains living microorganisms which, when applied to seed, plant surfaces or soil, colonizes the rhizosphere and/or the interior of the plant and promotes growth by enhancing the supply or availability of primary nutrients to the host plant [189]. Increasing concern over harmful effect of chemical fertilizers on environment and its high production cost make researchers attracted towards the utilization of microbial inoculants as biofertilizer, which has been reported as cost-effective and eco-friendly means of alternative to mineral fertilizers to enhance the yield and plant growth in sustainable agriculture [190]. Although a lot of bacterial isolates have been identified as plant growth promoters, extensive commercial application of these strains as biofertilizer is still limited [191]. Lack of consistent responses in different host cultivars under field conditions is considered as one of the major causes of the limited commercial utilization of biofertilizers [192]. However, application of a number of biofertilizers has been reported in numerous articles [191, 193, 194, 195, 196, 197]. For example, Azospirillum, one of very well-studied PGPR known for its N-fixing and phytohormone production ability, is regarded as safest bacteria which heads the list of bacteria used as a biofertilizer at commercial level for various crops, including wheat and rice [189, 193, 198, 199, 200]. However, a recent review [200] on this organism discussed its use as a commercial biofertilizer for different crops. In addition, the genus Azotobacter which has the ability to fix atmospheric nitrogen and synthesize plant hormones viz., indole acetic acid (IAA), gibberellins (GA) and cytokinins [201] is used as a biofertilizer for different crops such as wheat, oat, barley, mustard, rice, linseeds, sunflower, castor, maize, sorghum, cotton, jute, sugar beets, tobacco, tea, coffee, rubber and coconuts [202]. Furthermore, an investigation carried out for 2 years with the application of biofertilizers originating from a mixture of phytohormone producing Bacillus isolates exhibited increased plant growth and productivity [203].


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Moreover, in 2005, the US market has registered ten products, namely, Bioyield, Companion, EcoGuard, HiStick N/T, Kodiak, Mepplus, Serenade, Sonata, Subtilex, Yield-Shield based on the genus Bacillus. Hasnain and Sabri (1996) [204] reported that bacterization of wheat with Pseudomonas spp. enhanced plant growth by decreasing plant uptake of toxic ions and increasing the auxin content of wheat grown in Pakistan. Interestingly, phytohormones such as indole-3-acetic acid (IAA) and cytokinins have also been shown to play a key role in pathogenecity of gallforming and other phytopathogenic bacteria [205, 206, 207]. For instance, production of IAA has been reported to be important for pathogenecity of Pseudomonas syringae pv. Savastanoi, Agrobacterium tumefaciens and A. rhizogenes [208]. The ability to induce hypertrophic growth of Pseudomonas syringae pv. Savastanoi, which causes galls or knots on stems and leaves of infected host plants, is dependent on IAA synthesis by the pathogen [209, 210, 211]. Similarly, IAA encoding genes has also been shown to be essential for tumor formation and for induction of tumors and roots by Agrobacterium tumefaciens [212] and A. rhizogenes [213], respectively. In addition, genes specifying IAA [214] and a locus conferring cytokinin biosynthesis [133] have been isolated from Erwinia herbicola pv. Gypsophilae, which induces gall formation in Gypsophila paniculata (baby’s-breath) plants [215, 216], whereas another pathovar of E. herbicola is found to be pathogenic on table beet as well as gypsophila [217]. Therefore, although application of phytohormone producing microbial bioinoculants offers undoubted economic and environmental benefits, selection of species must be very carefully done to ensure safe biofertilizers production.

CONCLUSION AND FUTURE PERSPECTIVE The complexity of multitrophic interactions is a central theme as it is the potential for novel applied solutions to agricultural problems and concerns, such as rhizobacteria induced plant growth and stress tolerance. Plantassociated bacteria exert profound effects on growth and development of plants through various means including production and secretion of phytohormones. Probably acquired through horizontal gene transfer, the trait plant hormone production by bacteria significantly influences various metabolic and signaling pathways. The importance of both direct and, especially, indirect mechanisms of complex signaling involving phytohormones and quorum sensing is recognized repeatedly.

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The impact of molecular research such as transcriptional profiling and knockout mutants to unravel both signaling and metabolism [218] would give us a glimpse of the cutting-edge in present and the future [219]. Recent advances in genomic and postgenomic research would lead to better understanding the biosynthetic pathways of phytohormones in bacteria and elucidate the roles of these signaling substances in plant-bacteria and bacteriabacteria interactions. It is expected that isolation of elite strains of phytohormone producing bacteria, improvement of their desired traits through genetic engineering and apply them in crop production would significantly reduce the use of hazardous synthetic chemicals in agriculture. Reduction of synthetic agrochemicals by plant growth promoting bacteria not only enhance crop production but also reduce environmental pollution, which is badly needed for sustainable agriculture and food security.

ACKNOWLEDGMENTS We are thankful to the World Bank for funding this work through a subproject CP # 2071 of Higher Education Quality Enhancement Project (HEQEP) to the Department of Biotechnology of Bangabandhu Sheikh Mujibur Rahman Agricultural University, Bangladesh.

REFERENCES [1]

[2] [3] [4] [5]

Santner, A., Calderon-Villalobos, L. I. A. and Estelle, M. (2009). Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol., 5, 301-307. Went, F. W. and Thimann, K. V. (1937). Phytohormones. New York, The Macmillan Company. Darwin, C. R. and Darwin, F. (1980). The power of movement in plants. London, John Murray. von Sachs, J. (1887). Lectures on the physiology of plants. Oxford, Clarendon Press. Frébort, I., Kowalska, M., Hluska, T., Frébortová, J. and Galuszka, P. (20110. Evolution of cytokinin biosynthesis and degredation. J. Exp. Bot., 62, 2431-2452.

Promotion of Plant Growth by Phytohormone Producing Bacteria [6] [7] [8]

[9] [10]

[11]

[12]

[13]

[14]

[15]

[16] [17]

[18]

25

Kende, H. and Zeevaart, J. A. D. (1997). The five “classical” plant hormones. Plant Cell, 9, 1197-1210. Davies, P. J. (2004). Plant hormones: Biosynthesis, signal transduction, action! Springer Netherlands. UN DESA. (2013). World population prospects: 2013. Department of Economic and Social Affairs, Population Division. United Nations, New York. FAO. (2009). How to feed the world in 2050. Food and Agriculture Organizations of the United Nations. Bumb, B. L. and Baanante, C. A. (1996). World trends in fertilizer use and projections to 2020. International Food Policy Research Institute, Washington DC. Frink, C. R., Waggoner, P. E. and Ausubel, J. H. (1999). Nitrogen fertilizer: retrospect and prospect. Proc. Natl. Acad. Sci. US, 96, 11751180. Pinstrup-Anderson, P., Pandya-Lorch, R. and Rosegrant, M. W. (1997). The world food situation: Recent developments, emerging issues, and long-term prospects. Vision 2020: Food policy report (p. 36). International Food Policy Research Institute, Washington DC. Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W. H., Simberloff, D. and Swackhamer, D. (2001). Forecasting agriculturally driven global environmental change. Science, 292, 281-284. Kloepper, J. W. and Schroth, M. N. (1978). Plant growth promoting rhizobacteria on radishes. In: Proceedings of the 4th International Conference on plant pathogenic bacteria, INRA, Angers, France, 2, 879-882. Bashan, Y. and de Bashan, L. E. (2005). Fresh-weight measurements of roots provide inaccurate estimates of the effects of plant growthpromoting bacteria on root growth: a critical examination. Soil Biol. Biochem., 37, 1795-1804. Glick, B. R. (2012). Plant growth promoting rhizobacteria: mechanisms and applications. Scientifica. doi: 10.6064/2012/963401. Salamone, I. E. G., Hynes, R. K. and Nelson, L. M. (2001). Cytokinin production by Plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol., 47, 404-411. Joo, G. J., Kang, S. M., Hamayun, M., Kim, S. K., Na, C. I., Shin, D. H. and Lee, I. J. (2009). Burkholderia sp. KCTC 11096BP as a newly isolated gibberellins producing bacterium. J. Microbiol., 47, 167-171.

26


[19] Patten, C. L. and Glick, B. R. (2002). Role of Pseudomonas putida indole-acetic acid in development of the host plant root system. Appl. Environ. Microbiol., 68, 3795-3801. [20] Nieto, K. F. and Frankenberger, W. T. Jr. (1989). Biosynthesis of cytokinins by Azotobacter chroococcum. Soil Biol. Biochem., 21, 967972. [21] Timmusk, S., Nicander, B., Granhall, U. and Tillberg, E. (1999). Cytokinin production by Paenobacillus polymyxa. Soil Biol. Biochem., 31, 1847-1852. [22] Atzorn, R., Crozier, A., Wheeler, C. T. and Sandberg, G. (1988). Production of gibberellins and indole-3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots. Planta, 175, 532-538. [23] Lorteau, M. A., Ferguson, B. J. and Guinel, F. C. (2001). Effects of cytokinin on ethylene production and nodulation in pea (Pisum sativum cv. Sparkle). Physiol. Plant, 112, 421-428. [24] Kang, S. M., Joo, G. J., Hamayun, M., Shin, D. H., Kim, H. Y., Hong, J. K. and Lee, I. J. (2009). Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol. Lett., 31, 277-281. [25] Jha, P. N. and Kumar, A. (2007). Endophytic colonization of Typha australis by a plant growth-promoting bacterium Klebsiella oxytoca strain GR-3. J. App. Microbiol., 103, 1311-1320. [26] Mia, M. A. B., Hossain, M. M., Shamsuddin, Z. H. and Islam, M. T. (2013). Plant-associated bacteria in nitrogen nutrition in crops, with special reference to rice and banana. In: D. K. Maheshwari, M. Saraf and A. Aeron (Eds.), Bacteria in agrobiology: crop productivity (pp. 97126). Berlin Heidelberg: Springer. [27] Islam, M. T., Deora, A., Hashidoko, Y., Rahman, A., Ito, T. and Tahara, S. (2007). Isolation and identification of potential phosphate solubilizing bacteria from the rhizoplane of Oryza sativa L. cv. BR29 of Bangladesh. Z Naturforsch, 62, 103-110. [28] Islam, M. T. and Hossain, M. M. (2012). Plant probiotics in phosphorus nutrition in crops, with special reference to rice. In: D. K. Maheshwari (Ed.), Bacteria in agrobiology: plant probiotics (pp. 325-363). Berlin Heidelberg: Springer. [29] Phi, Q-T., Yu-Mi, P., Keyung-Jo, S., Choong-Min, R., Seung-Hwan, P., Jong-Guk, K. and Sa-Youl, G. (2010). Assessment of root-associated


[30]

[31]

[32]

[33]

[34]

[35]

[36]

[37] [38]

[39] [40]

27

Paenobacillus polymyxa groups on growth promotion and induced systemic resistance in pepper. J. Microbiol. Biotechnol., 20, 1605-1613. Islam, M. T., Hashidoko, Y., Deora, A., Ito, T. and Tahara, S. (2005). Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soil borne Peronosporomycetes. Appl. Environ. Microbiol., 71, 3786-3796. Islam, M. T. (2008). Disruption of ultra-structure and cytoskeleton network is involved with biocontrol of damping-off pathogen Aphanomyces cochliodes by Lysobacter sp. strain SB-K88. Biocontrol., 46, 312-321. Islam, M. T. (2010). Mode of antagonism of a biocontrol bacteria Lysobacter sp. strain SB-K88 toward a damping off pathogen Aphanomyces cochliodes by. World J. Microbiol. Biotechnol., 26, 629637. Islam, M. T. (2011). Potential for biological control of plant diseases by Lysobacter sp. With special reference to strain SB-K88. In: D. K. Maheshwari (Ed.), Bacteria in agrobiology: plant growth responses (pp. 335-363). Berlin Heidelberg: Springer. Wani, P. A. and Khan, M. S. (2010). Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem. Toxicol., 48, 3262-3267. Islam, M. T. and Hossain, M. (2013). Biological control of Peronosporomycetes phytopathogens by bacterial antagonist. In: D. K. Maheshwari (Ed.), Bacteria in agrobiology: disease management (pp. 167-218). Berlin Heidelberg: Springer. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S. and Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Ann. Rev. Plant Biol., 57, 233-266. Lugtenberg, B. and Kamilova, F. (2009). Plant-growth-promoting rhizobacteria. Ann. Rev. Microbiol., 63, 541-556. Hiltner, L. (1904). Über neue erfahrungen und probleme auf dem gebiet der bodenbakteriologie unter besonderer berüksichtigung der gründüngung und brache. Arb Dtsch Lanwirt Ges, 98, 59-78. Walker, T. S., Bais, H. P., Grotewold, E. and Vivanco, J. M. (2003). Root exudation and rhizosphere biology. Plant Physiol., 132, 44-51. Ashrafuzzaman, M., Hossen, F. A., Ismail, M. R., Hoque, M. A., Islam, M. Z., Shahidullah, S. M. and Meon, S. (2009). Efficiency of plant

28

[41]

[42]

[43]

[44]

[45]

[46]

[47]

[48]

[49]

[50]

[51]

Mohibul Alam Khan, Amena Khatun and Tofazzal Islam growth-promoting rhizobacteria (PGPR) for the enhancement of rice growth. African J. Biotechnol., 8, 1247-1252. Chaiharn, M. and Lumyong, S. (2011). Screening and optimization of indole-3-acetic acid production and phosphate solubilization from rhizobacteria aimed at improving plant growth. Curr. Microbiol., 62, 173-181. Iqbal, A. and Hasnain, S. (2013). Auxin producing Pseudomonas strains: biological candidates to modulate the growth of Triticum aestivum beneficially. American J. Plant Sci., 4, 1693-1700. Priya, S., Panneerselvam, T. and Sivakumar, T. (2013). Evaluation of indole-3-acetic acid in phosphate solubilizing microbes isolated from rhizosphere soil. Int. J. Curr. Microbiol. App. Sci., 2, 29-36. Abd-Alla, M. H., El-Sayed, E-S. A. and Rasmey, A-H. M. (2013). Indole-3-acetic acid (IAA) production by Streptomyces atrovirens isolated from rhizospheric soil in Egypt. J. Biol. Earth Sci., 3, 81828193. Sivasankari, B., Kayikumar, N. and Anandharaj, M. (2013). Indole-3acetic acid production and enhanced plant growth promotion by indigenous bacterial species. J. Curr. Res. Sci., 1, 331-335. Yasmin, F., Othman, R., Sijam, K. and Saad, M. S. (2009). Characterization of beneficial properties of plant growth-promoting rhizobacteria isolated from sweet potato rhizosphere. African J. Microbiol. Res., 3, 815-821. Joseph, B., Patra, R. R. and Lawrence, R. (2007). Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int. J. Plant Prod., 2, 141-152. Mohite, B. (2013). Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J. Soil Sci. Plant Nutr., 13, 638-649. Lwin, K. M., Myint, M. M., Tar, T. and Aung, W. Z. M. (2012). Isolation of plant hormone (indole-3-acetic acid-IAA) producing rhizobacteria and study on their effects on maize seedling. Enginneering J., 16, 137-144. Hafeez, F. Y., Yasmin, S., Ariani, D., Rahman, M., Zafar, Y. and Malik, K. A. (2006). Plant growth-promoting bacteria as biofertilizer. Agron. Sustain. Dev., 26, 143-150. Gutierrez, C. K., Matsui, G. Y., Lincoln, D. E. and Lovell, C. R. (2009). Production of the phytohormone indole-3-acetic acid by estuarine species of the genus Vibrio. Appl. Environ. Microbiol., 75, 2253-2258.


29

[52] Kuklinsky-Sobral, J., Araújo, W. L., Mendes, R., Geraldi, I. O., Pizzirani-Kleiner, A. A. and Azevedo, J. L. (2004). Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol., 6, 1244-1251. [53] Bhore, S. J., Nithya, R. and Loh, C. Y. (2010). Screening of endophytic bacteria isolated from leaves of Sambung Nyawa [Gynura procumbens (Lour.) Merr.] for cytokinin-like compounds. Bioinformation, 5, 191197. [54] Srinivasan, R., Alagawadi, A. R., Yandigeri, M. S., Meena, K. K. and Saxena, A. K. (2012). Characterization of phosphate-solubilizing microorganisms from salt-affected soils of India and their effect on growth of sorghum plants [Sorghum bicolor (L.) Moench]. Ann. Microbiol., 62, 93-105. [55] Pradeepa, V. and Jennifer, M. (2013). Screening and characterization of endophytic bacteria isolated from Tabernaemontana divaricata plant for cytokinin production. Advanced Biotech., 13, 12-17. [56] DeVay, J. E., Lukezic, F. L., Sinden, S. L., English, H. and Coplin, D. L. (1968). A biocide produced by pathogenic isolates of Pseudomonas syringae and its possible role in bacterial canker disease of peach trees. Phytopathology, 58, 95-101. [57] Bric, J. M., Bostock, R. M. and Silverstone, S. E. (1991). Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl. Environ. Microbiol., 57, 535-538. [58] Shrivastava, U. P. and Kumar, A. (2011). A simple and rapid plate assay for the screening of indole-3-acetic acid (IAA) producing microorganisms. Int. J. Appl. Bio. Pharma. Tech., 2, 120-123. [59] Mitchell, J. W. and Brunstetrer, B. C. (1939). Colorimetric methods for the quantitative estimation of indole(3)acetic acid. Bot. Gaz., 100, 802816. [60] Tang, Y. W. and Bonner, J. (1947). The enzymatic inactivation of indole acetic acid. Arch. Biochem., 13, 11-25. [61] Gordon, S. A. and Weber, R. P. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiol., 26, 192-195. [62] Khatun, A., Islam, S. M. N., West, H. M., Hasan, M. and Islam, M. T. (2013). Epiphytic bacteria isolated from chili inhibit mycelial growth and impair motility of the zoospores of late blight pathogen Phytophthora capsici (unpublished).

30


[63] Brown, M. E. and Burlingham, S. K. (1968). Production of plant growth substances by Azotobacter chlorococum. J. Gen. Microbiol., 53, 135144. [64] Fletcher, R. A. and Mccullagh, D. (1971). Cytokinin-induced chlorophyll formation in cucumber cotyledons. Planta, 101, 88-90. [65] Brenner, M. L., Andersen, C. R., Ciha, A. J., Mondal, M. and Brun, W. (1976). Relationship of endogenous plant hormone content to changes in source-sink relationships. In: P-E. Pilet (Ed.), 9th International conference on plant growth substances, Lausanne (pp. 49-50). [66] Fletcher, R. A., Kallidumbil, V. and Steele, P. (1982). An improved bioassay for cytokinins using cucumber cotyledons. Plant Physiol., 69, 675-677. [67] Hussain, A. and Hasnain, S. (2009). Cytokinin production by some bacteria: its impact on cell division in cucumber cotyledons. African J. Microbiol. Res., 3, 704-712. [68] Vandamme, P., Pot, B., Gillis, M., De Vos, P., Kersters, K. and Swings, J. (1996). Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Mol. Biol. Rev., 60, 407-438. [69] de Vos, P., Garrity, G., Jones, D., Krieg, N. R., Ludwig, W., Rainey, F. A., Schleifer, K-H. and Whitman, W. B. (2009). Bergey’s manual of systematic bacteriology. Volume 3: The Firmicutes. (2nd ed.) Williams and Wilkins. [70] Naik, P. R., Raman, G., Narayanan, K. B. and Sakthivel, N. (2008). Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiol., 8, 230-243. [71] Eisen, J. A. (1995). The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J. Mol. Evol., 41, 1105-1123. [72] Ludwig, W., Strunk, O., Klugbauer, S., Klugbauer, N., Weizenegger, N., Neumaier, J., Bachleitner, M. and Schleifer, K.-H. (1998). Bacterial phylogeny based on comparative sequence analysis. Electrophoresis, 19, 554-568. [73] Chen, Y. P., Rekha, P. D., Arun, A. B., Shen, F. T., Lai, W. A. and Young, C. C. (2006). Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl. Soil Ecol., 34, 33-41. [74] Selvakumar, G., Joshi, P., Suyal, P., Mishra, P. K., Joshi, G. K., Bisht, J. K., Bhatt, J. C. and Gupta, H. S. (2011). Pseudomonas lurida M2RH3


[75]

[76]

[77]

[78]

[79]

[80]

[81]

[82] [83]

31

(MTCC 9245), a psychrotolerant bacterium from the Uttarakhand Himalayas, solubilizes phosphate and promotes wheat seedling growth. World J. Microbial Biotechnol., 27, 1129-1135. Kang, S-M., Khan, A. L., Hamayun, M., Hussain, J., Joo, G-J., You, YH., Kim, J-G. and Lee, I-J. (2012). Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J. Microbiol., 50, 902-909. Peix, A., Rivas, R., Mateos, P. F., Martıńez-Molina, E., Rodrı´guezBarrueco, C. and Vela´zquez, E. (2003). Pseudomonas rhizosphaerae sp. nov., a novel species that actively solubilizes phosphate in vitro. Int. J. Syst. Evol. Microbiol., 53, 2067-2072. Peix, A., Rivas, R., Santa-Regina, I., Mateos, P., Martıńez-Molina, E., Rodriguez-Barrueco, C. and Vela´zquez, E. (2004). Pseudomonas lutea sp. nov., a novel phosphate-solubilizing bacterium isolated from the rhizosphere of grasses. Int. J. Syst. Evol. Microbiol., 54, 847-850. Rivas, R., Trujillo, M. E., Sańchez, M., Mateos, P. F., MartıńezMolina, E. and Vela´squez, E. (2004). Microbacterium ulmi sp. nov. a xylanolytic, phosphate-solubilizing bacterium isolated from sawdust of Ulmus nigra. Int. J. Syst. Evol. Microbiol., 54, 513-517. Wang, L-T., Lee, F-L., Tai, C-J. and Kasai, H. (2007). Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA-DNA hybridization in the Bacillus subtilis group. Int. J. Syst. Evol. Microbiol., 57, 1846-1850. Cerritos, R., Vinuesa, P., Eguiarte, L. E., Herrera-Estrella, L., AlcarazPeraza, L. D., Arvizu-Go´mez, J. L., Olmedo, G., Ramirez, E., Siefert, J. L. and Souza, V. (2008). Bacillus coahuilensis sp. nov., a moderately halophilic species from a desiccation lagoon in the Cuatro Cieńegas Valley in Coahuila, Mexico. Int. J. Syst. Evol. Microbiol., 58, 919-923. Peix, A. and Martinez-Molina, E. (2002). Molecular methods for biodiversity analysis of PSB. In: First meeting on microbial phosphate solubilization. Salamanca, Spain, 16-19 July. Costacurta, A. and Vanderleyden, J. (1995). Synthesis of phytohormones by plant-associated bacteria. Crit. Rev. Microbiol., 21, 1-18. Lindow, S. E., Desurmont, C., Elkins, R., McGourty, G. and Clark, E. (1998). Occurrence of indole-3-acetic acid-producing bacteria on pear trees and their association with fruit russet. Phytopathol., 88, 1149-1157.

32


[84] Spaepen, S., Vanderleyden, J. and Remans, R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev., 31, 425-448. [85] Hoffman, M. T., Gunatilaka, M. K., Wijeratne, K., Gunatilaka, L. and Arnold, A. E. (2013). Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS ONE, 8, e73132. [86] Chunmei, G., Xingchun, W., Jian, F. and Sulei H. (2014). Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of ABI5 protein in Arabidopsis. Plant Physiol., 113, 234-740. [87] Cassán, F., Diego, P., Verónica, S., Oscar, M. and Claudio, P. (2011). Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Euro J. Soil Biol., 47, 214. [88] Bákonyi, N., Bott, S., Gajdos, É., Szabó, A., Jakab, A., Tóth, B., Makleit, P. and Veres, S. Z. (2013). Using biofertilizer to improve seed germination and early development of maize. Pol. J. Environ. Stud., 22, 1595-1599. [89] Werner, T., Motyka, V., Strnad, M. and Schmulling, T. (2001). Regulation of plant growth by cytokinin. Proc. Natl. Acad. Sci. US, 98, 10487-1049. [90] Yang, J., Zhang, J., Huang, Z., Wang, Z., Zhu, Q. and Liu, L. (2002). Correlation of cytokinin levels in the endosperm and roots with cell number and cell division activity during endosperm development in Rice. Ann. Bot., 90, 369-377. [91] Glick, B. R. (1995). The enhancement of plant growth by free living bacteria. Can. J. Microbiol., 41, 109-117. [92] Chakraborty, U., Chakraborty, B. and Basnet, M. (2006). Plant growth promotion and induction of resistance in Camellia sinensis by Bacillus megaterium. J. Bas. Microbiol., 46, 186-195. [93] Ortíz-Castro, R., Valencia-Cantero, E. and López-Bucio, J. (2008). Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal. Behav., 3, 263-265. [94] Ryu, C., Farag, M. A., Hu, C., Reddy, M. S., Wei, H., Pare, P. W. and Kloepper, J. W. (2003). Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci., 100, 4927-4932. [95] Hedden, P. and Kamiya, Y. (1997). Gibberellin biosynthesis: enzymes, genes, and their regulation. Ann. Rev. Plant Phys., 48, 431-460.


33

[96] Ma, W., Sebestianova, S. B., Sebestian, J., Burd, G. I., Guinel, F. C. and Glick, B. R. (2003). Prevalence of 1- aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. A van Leeuw, 83, 285-91. [97] Maren, L. F., Stephanie, S. P., Scott, C., Stark, E. J., vonWettberg., Joel, L. S. and Martinez-Romero, E. (2011). Microbially mediated plant functional traits. Ann. Rev. Ecol. Evol. Syst., 42, 23-46. [98] Spaepen, S., Dobbelaere, S., Croonenborghs, A. and Vanderleyden, J. (2008). Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil, 312, 15-23. [99] Dazzo, F. B., Yanni, Y. G., Rizk, R., De Bruijn, F. J., Rademaker, J., Squartini, A., Corich, V., Mateos, P. and Martinez-Molina E. (2000). Progress in multinational collaborative studies on the beneficial association between Rhizobium Ieguminosarum by trifolii and rice. In: J. K. Ladha and P. M. Reddy (Eds.) The quest for nitrogen fixation in rice (pp. 167-189). IRR1, Los Banos, Philippines. [100] Pacovsky, R. S., Paul, E. A. and Bethlenfalvay, G. J. (1985). Nutrition of sorghum plants fertilized with nitrogen or inoculated with Azospirillum brasilense. Plant Soil, 85, 145-148. [101] Çakmakçi, R., Dönmez, M. F. and Ümmügülsüm, E. (2007a). The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turk. J. Agric. For., 31, 189-199. [102] Jay, P. V., Janardan, Y., Kavindra, N. T. and Ashok, K. (2013). Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol. Eng., 51, 282-286. [103] Morshed, M. H., Hossain, M. S., Ibrahim, M., Shafique, M. Z. and Helali, M. O. H. (2005). Bacteria killing kinetics of the four plant hormones. Pak. J. Biol. Sci., 8, 1025-1029. [104] Romero, A. M., Correa, O. S., Moccia, S. and Rivas, J. G. (2003). Effect of Azospirillum-mediated plant growth promotionon the development of bacterial diseases on fresh-market and cherry tomato. J. Appl. Microbiol., 95, 832-838. [105] Hayat, R., Ali, S., Amara, U., Khalid, R. and Ahmed, I. (2010). Soil beneficial bacteria and their role in plant growth promotion: a review. Ann. Microbiol., 60, 579-598. [106] Hao, Y., Charles, T. C. and Glick, B. R. (2007). ACC deaminase from plant growth-promoting bacteria affects crown gall development. Can. J. Microbiol., 53, 1291-1299.

34


[107] Johnson, N. D., Liu, B. and Bentley, B. L. (1987). The effects of nitrogen fixation, soil nitrate, and defoliation on the growth, alkaloids, and nitrogen levels of Lupinus succulentus (Fabaceae). Oecologia, 74, 425-431. [108] Kevin, V. J. (2003). Plant growth promoting rhizobacteria as biofertilizer. Plant Soil, 255, 571-586. [109] Khakipour, N., Khavazi K., Mojallali, H., Pazira, E. and Asadirahmani, H. (2008). Production of auxin hormone by fluorescent pseudomonads. American-Eurasian J. Agric. Environ. Sc., 4, 687-692. [110] Yobo, K. S., Laing, M. D. and Hunter, C. H. (2004). Effect of commercially available rhizobacteria strains on growth and production of lettuce, tomato and pepper. S. African J. Pl. Soil., 21, 230-235. [111] Lucangeli, C. and Bottini, R. (1997). Effects of Azospirillum spp. on endogenous gibberellin contentand growth of maize (Zea mays L.) treated with uniconazole. Symbiosis, 23, 63-72. [112] Piccoli, P., Lucangeli, D., Schneider, G. and Bottini, R. (1997). Hydrolysis of Gibberellin A20-Glucoside and [17, 17-2H2] Gibberellin A20-glucosylester by Azospirillum lipoferum cultured in a nitrogen-free biotin-based chemically-defined medium. Plant Growth Regul., 23, 179182. [113] Cassán, F., Bottini, R., Schneider, G. and Piccoli, P. (2001). Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of GA20 and metabolize the resultant aglycones to GA1 inseedlings of rice dwarf mutants. Plant Physiol., 125, 2053-2058. [114] Burd, G., Dixon, D. G. and Glick, B. R. (2000). Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol., 46, 237-245. [115] Biswas, J. C., Ladha, J. K., Dazzo, F. B., Yanni, Y. G. and Rolf, B. G. (2000). Rhizobial inoculation influences seedling vigor and yield of rice. Agron. J., 90, 880-886. [116] Zahir, Z. A., Abbas, S. A., Khalid, M. and Arshad, M. (2000). Substrate dependent microbially derived plant hormones for improving growth of maize seedlings. Pak. J. Biol. Sci., 3, 289-291. [117] Yanni, Y. G., Rizk, R. Y., El-Fattah, A. F. K., Squartini, A., Corich, V., Giacomini, A., de Bruijn, F., Rademaker, J., Maya-Flores, J., Ostrom, P., Vega-Hernandez, M., Hollingsworth, R.I., Martinez- Molina, E., Ninke, K., Philip-Hollingsworth, S., Mateos, P. F., Velasquez, E., Triplett, E., Umali-Garcia, M., Anarna, J. A., Rolfe, B. G., Ladha, J. K., Hill, J., Mujoo, R. and Dazzo, F. B. (2001). The beneficial plant growth-


35

promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust. J. Plant Physiol., 28, 845-870. [118] Dey, R., Pal, K. K., Bhatt, D. M. and Chauhan, S. M. (2004). Growth promotion and yield enhancement of peanut (Arachis hypogaea L) by application of plant growth promoting rhizobacteria. Microbiol. Res., 159, 371-394. [119] Thakuria, D., Taleekdar, N. C., Goswami, C., Hazarika, S., Boro, R. C. and Khan, M. R. (2004). Characterization and screening of bacteria from rhizosphere of rice grown in acidic soils of Assam. Curr. Sci., 86, 978985. [120] Muratova, A. Y., Turkovskaya, O. V., Antonyuk, L. P., Makarov, O. E., Pozdnyakova, L. I. and Ignatov, V. V. (2005). Oil-oxidizing potential of associative rhizobacteria of the genus Azospirillum. Microbiol., 74, 210215. [121] Ahmad, F., Ahmad, I. and Khan, M. S. (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. [122] Roesti, D., Guar, R., Johri, B. N., Imfeld, G., Sharma, S., Kawaljeet, K. and Aragno, M. (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. [123] Çakmakçi, R., Erat, M., Erdoğan, Ü. G. and Dönmez, M. F. (2007b). 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. [124] Chandra, S., Choure, K., Dubey, R. C. and Maheshwari, D. K. (2007). Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling inhibits Sclerotiniasclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz. J. Microbiol., 38, 124-130. [125] Dell’Amico, E., Cavalca, L. and Andreoni, V. (2008). Improvement of Brassica napus growth under cadmium stress by cadmium resistant rhizobacteria. Soil Biol. Biochem., 40, 74-84. [126] Beneduzi, A., Peres, D., Vargas, L. K., Bodanese-Zanettini, M. H. and Passaglia, L. M. P. (2008). Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing Bacilli isolated from rice fields in South Brazil. Appl. Soil Ecol., 39, 311-320.

36


[127] Zarrin, K. and Sharon, L. D. (2010). Characterization of bacterial endophytes of sweet potato plants. Plant Soil, 322, 197-207. [128] Kucey, R. M. N. (1988). Plant growth-altering effects of Azospirillum brasilense and Bacillus C-11-25 on two wheat cultivars. J. Appl. Bacteriol., 64, 187-196. [129] Probanza, A., García, J. A. L., Palomino, M. R., Ramos, B. and Manero, F. J. G. (2002). Pinuspinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CECT 5106 and B. pumilus CECT 5105). Appl. Soil Ecol., 20, 75-84. [130] Joo, G. J., Kim, Y. M., Kim, J. T., Rhee, I. K., Kim, J. H. and Lee, I. J. (2005). Gibberellins-producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J. Microbiol., 43, 510-515. [131] Sang-Mo, K., Khan, A. L., Hamayun, M., Hussain, J., Joo, J-G., You, YH., Kim, J-G. and Lee, I-J. (2012). Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J. Microbiol., 50, 902-909. [132] Tien, T. M., Gaskin, M. H. and Hubbell, D. H. (1979). Plant growth substances produced by Azospirillumbrasilenseand their effect on the growth of pearl millet (PennisetumamericanumL). Appl. Environ. Microbiol., 37, 1016-1024. [133] Lichter, A., Barash, I., Valinsky, L. and Manulis, S. (1995). The genes involved in cytokinin biosynthesis in Erwiniaherbicola pv. gypsophilae, characterization and role in gall formation. J. Bacteriol., 177, 44574465. [134] Patten, C. L. and Glick, B. R. (1996). Bacterial biosynthesis of indole-3acetic acid. Can. J. Microbial., 42, 207-220. [135] Comai, L. and Kosuge, T. (1982). Cloning characterization of iaaM, a virulence determinant of Pseudomonas savastanoi. J. Bacteriol., 149, 40-46. [136] Yamada, T., Palm, C., Brooks, B. and Kosuge, T. (1985). Nucleotide sequences of the Pseudomonas savastanoi indoleacetic acid genes show homology with Agrobacterium tumefaciens T-DNA. Proc. Natl. Acad. Sci., 82, 6522-6526. [137] Taiz, L. and Zeiger, E. (1998). Plant Physiology (2nd ed.). Sinauer Associates, Inc., Sunderland, Mass.


37

[138] Koga, J., Adachi, T. and Hidaka, H. (1991). Molecular cloning of the gene for indolepyruvate decarboxylase from Enterobacter cloacae. Mol. Gen. Genet., 226, 10-16. [139] Costacurta, A., Keijers, V. and Vanderleyden, J. (1994). Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3pyruvate decarboxylase gene. Mol. Gen. Genet., 243, 463-472. [140] Brandl, M., Clark, E. M. and Lindow, S. E. (1996). Characterization of the indole-3-acetic acid (IAA) biosynthetic pathway in an epiphytic strain of Erwinia herbicola and IAA production in vitro. Can. J. Microbiol., 42, 586-592. [141] Vereecke, D., Messens, E., Klarskov, K., Bruyn, A., Montagu, M. and Goethals, K. (1997). Patterns of phenolic compounds in leafy galls of tobacco. Planta, 201, 342-348. [142] Manulis, S., Haviv-Chesner, A., Brandl, M. T., Lindow, S. E. and Barash, I. (1998). Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Am. Phytopath. Society, 11, 634-642. [143] Bartling, D., Seedorf, M., Schmidt, R. and Weiler, E. (1994). Molecular characterization of two cloned nitrilases from Arabidopsis thaliana: key enzymes in biosynthesis of the plant hormone indole-3-acetic acid. Proc. Natl. Acad. Sci. US, 91, 6021-6025. [144] Kobayashi, M., Suzuki, T., Fujita, T., Masuda, M. and Shimizu, S. (1995). Occurrence of enzymes involved in biosynthesis of indole-3acetic acid from indole-3-acetonitrile in plant-associated bacteria, Agrobacterium and Rhizobium. Proc. Natl. Acad. Sci. US, 92, 714-718. [145] Oberhänsli, T., Défago, G. and Haas, D. (1991). Indole-3-acetic acid (IAA) synthesis in the biocontrol strain CHAO of Pseudomonas fluorescens, role of tryptophan side chain oxidase. J. Gen. Microbiol., 137, 2273-2279. [146] Zaidi, A., Khan, M. S., Ahemad, M. and Oves, M. (2009). Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung., 56, 263-284. [147] Spaepen, S. and Vanderleyden, J. (2011). Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol., 3, a001438. doi; 10. 1101/cshperspect.a001438. [148] Williams, P. M. and de Mallorca. S. (1982). Abscisic acid and gibberellin-like substances in roots and root nodules of Glycine max. Plant Soil, 65, 19-26.

38


[149] Janzen, R. A., Rood, S. B., Dormaar, J. F. and McGill, W. B. (1992). Azospirillum brasilense produces gibberellin in pure culture on chemical-defined medium and in co-culture on straw. Soil Biol. Biochem., 24, 1061-1064. [150] Bastián, F., Cohen, A., Piccoli, P., Luna, V., Baraldi, R. and Bottini, R. (1998). Production of indole-3- acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillumseropedicae in chemically-defined culture media. Plant Growth Reg., 24, 7-11. [151] Gutierrez-Manero, F. J., Ramos-Solano, B., Probanza, A., Mehouachi, J., Tadeo, F. R. and Talon, M. (2001). The plant-growth-promoting rhizobacteria Bacillus pumilis and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant, 111, 206211. [152] MacMillan, J. (2001). Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Reg., 20, 387-442. [153] Mitter, N., Srivastava, A. C., Renu, A. S., Sarbhoy, A. K. and Agarwal, D. K. (2002). Characterization of gibberellin producing strains of Fusarium moniliforme based on DNA polymorphism. Mycopathologia, 153, 187-193. [154] Bottini, R., Cassan, F. and Piccoli, P. (2004). Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol., 65, 497-503. [155] Tsavkelova, E. A., Klimova, S. Y., Cherdyntseva, T. A. and Netrusov, A. I. (2006). Microbial producers of plant growth stimulators and their practical use: a review. Appl. Biochem. Microbiol., 42, 117-126. [156] Boiero, L., Perrig, D., Masciarelli, O., Penna, C., Cassan, F. and Luna, V. (2007). Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl. Microbiol. Biotechnol., 74, 874-880. [157] Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Ann. Rev. Plant Biol., 59, 225-251. [158] Tudzynski, B. (2005). Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology. Appl. Microbiol. Biotechnol., 66, 597-611. [159] Fischbach, M. A. and Clardy, J. (2007). One pathway, many products. Nat. Biol. Chem., 3, 353-355. [160] Morrone, D., Chambers, J., Lowry, L., Kim, G., Anterola, A., Bender, K. and Peters, R. J. (2009). Gibberellin biosynthesis in bacteria: separate


39

ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum. FEBS Lett., 583, 475-480. [161] Piccoli, P. and Bottini, R. (1996). Gibberellin production in Azospirillum lipoferum cultures is enhanced by light. Bio cell, 20, 185-190. [162] Piccoli, P. and Bottini, R. (1994). Effects of C/N relationships, N content, pH, and time of culture on growth and gibberellins production of Azospirillum lipoferum cultures. Symbiosis, 17, 229-236. [163] Piccoli, P., Masciarelli, O. and Bottini, R. (1999). Gibberellin production by Azospirillum lipoferum cultured in chemically-defined medium as affected by oxygen availability and water status. Symbiosis, 27, 135-146. [164] Hedden, P., Philips, A. L., Rojas, M. C., Carrere, E. and Tudzynski, B. (2001). Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? J. Plant Growth Regul., 20, 319-331. [165] Tully, R. E., van Berkum, P., Lovins, K. W. and Keister, D. L. (1988). Identification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum. Biochim. Biophys. Acta, 1398, 243-255. [166] Taller, B. J. and Wong, T. Y. (1989). Cytokinins in Azotobacter vinelandii culture medium. Appl. Environ. Microbiol., 55, 266-267. [167] Letham, D. S. and Palni, L. M. S. (1983). The biosynthesis and metabolism of cytokinins. Annu. Rev. Plant Physiol., 34, 163-197. [168] Barry, G. F., Rogers, S. G., Fraley, R. T. and Brand, L. (1984). Identification of a cloned cytokinin biosynthetic gene. Proc. Natl. Acad. Sci. US, 61, 4776-4780. [169] Heinemeyer, W., Buchmann, I., Tonge, D. W., Windass, J. D., AltMoerbe, J., Weiler, E. W., Botz, T. and Schroder, J. (1987). Two Agrobacterium tumefaciens genes for cytokinin biosynthesis: Ti plasmid-coded isopentenyltransferase adapted for function in prokaryotic or eukaryotic cells. Mol. Gen. Genet., 210, 257-262. [170] Akiyoshi, D. E., Klee, H., Amasino, R. M., Nester, E. W. and Gordon, P. M. (1984). T-DNA of Agrobacterium tumefaciens encodesan enzyme of cytokinin biosynthesis. Proc. Natl. Acad. Sci. US, 81, 5994-5998. [171] Ivanova, E. G., Doronina, N. V. and Ya, T. (2001). Aerobic methylobacteria are capable of synthesizing auxins. Mikrobiologiya, 70, 452-458. [172] Koenig, R. L., Morris, R. O. and Polacco, J. C. (2002). tRNA is the source of low-level trans-zeatin production in Methylobacterium spp. J. Bacteriol., 184, 1832-1842. [173] Morris, R. O., Blevins, D. G., Dietrich, J. T., Durley, R. C., Gelvin, S. B., Gray, J., Hommes, N. G., Kaminek, M., Mathesius, U., Meilan, R.,

40


Reinbott, T. M., Sayavedra-Soto, L. (1993). Cytokinins in plant pathogenic bacteria and developing cereal grains. Aust. J. Plant Physiol., 20, 621-637. [174] Powell, G. K. and Morris, R. O. (1986). Nucleotide sequence and expression of Pseudomonas savastanoi cytokinin biosynthetic gene: Homology with Agrobacterium tumefaciens tmr and tzs loci. Nucleic Acids Res., 14, 2555-2565. [175] Akiyoshi, D. E., Regier, D. A. and Gordon, M. P. (1989). Nucleotide sequence of the tzs gene from Pseudomonas solanacearum strain K60. Nucleic Acids Res., 17, 8886. [176] Crespi, M., Messens, E., Caplan, A. B., van Montagu, M. and Desomer, J. (1992). Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J., 11, 795-804. [177] Gray, J., Wang, J. and Gelvin, S. B. (1992). Mutation of the miaA gene of Agrobacterium tumefaciens results in reduced vir gene expression. J. Bacteriol., 174, 1086-1098. [178] Leveau, J. H. J. and Lindow, S. E. (2005). Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Appl. Environ. Microbiol., 71, 2365-2371. [179] Faure, D., Vereecke, D. and Leveau, J. H. J. (2009). Molecular communication in the rhizosphere. Plant Soil, 321, 279-303. [180] Shahab, S. and Ahmed, N. (2008). Effect of various parameters on the efficiency of zinc phosphate solubilization by indigenous bacterial isolates. Afr. J. Biotechnol., 7, 1543-1549. [181] Cornelissen, J. H. C., Lavorel, S., Garnier, E., Diaz, S. and Buchmann, N. (2003). A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aus. J. Bot., 51, 335380. [182] Friesen, M. L., Porter, S. S., Stark, S. C., von Wettberg, E. J., Sachs, J. L. and Martinez-Romero, E. (2012). Microbially mediated plant functional traits. Ann. Rev. Ecol. Evol. Syst., 42, 23-46. [183] Ribaudo, C. M., Krumpholz, E. M., Cassán, F. D., Botín, R., Cantore, M. L. and Curá, J. A. (2006). Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J. Plant Growth Regul., 24, 75-185. [184] Valverde, C. and Wall, L. G. (2005). Ethylene modulates the susceptibility of the root for nodulation in actinorhizal discariatrinervis. Physiol. Plant, 124, 121-131.


41

[185] Peters, N. K. and Crist-Estes, D. K. (1989). Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol., 91, 690-693. [186] Solans, M. (2007). Discariatrinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J. Basic Microbiol., 47, 243-250. [187] Solans, M., Vobis, G. and Wall, L. G. (2009). Saprophytic actinomycetes promote nodulation in Medicago sativa- Sinorhizobium meliloti symbiosis in the presence of high N. J. Plant Growth Regul., 28, 106-114. [188] Ansary,H . M., Rahmani,A . H., Ardakani,M . R., Paknejad,F ., Habibi , D. and Mafakheri ,S( .2012 .)Effect of Pseudomonas fluorescent on Proline and Phytohormonal status of Maize (Zea mays L.) under water deficit stress .Ann. Biol. Res., 2, 1054-1062. [189] Vessey, J. K. (2003). Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 255, 571-586. [190] Canbolat, M. Y., Barik, K. K., Cakmarci, R. and Sabin, F. (2006). Effects of mineral and biofertilizers on barley growth on compacted soil. Act. Agric. Scand., 56, 324-332. [191] Figueiredo, M. V. B., Seldin, L., de Araujo, F. F. and Mariano, R. L. R. (2010). Plant Growth Promoting Rhizobacteria: Fundamentals and Applications. In: D. K. Maheshwari, (Ed.), Plant growth and health promoting bacteria, microbiology monographs (pp. 21-43). [192] Remans, S., Blair, M. W., Manrique, G., Tovar, L. E., Rao, I. M., Croomenborghs, A., Torres, G. R., El-Howeity, M., Michiels, J. and Vanderleyden, J. (2008). Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil, 302, 149-161. [193] Fuentes-Ramirez, L. E. and Caballero-Mellado, J. (2005). Bacterial biofertilizer. In: Z. A. Siddiqui (Ed.), PGPR: Biocontrol and biofertilization, (pp. 143-172). [194] Bhardwaj, D., Ansari, M. W., Sahoo, R. K. and Tuteja, N. (2014). Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microbial Cell Factories, 13, 66-75. [195] Mazid, M. and Khan, T. A. (2014). Future of bio-fertilizers in indian agriculture: an overview. Int. J. Agri. Food Res., 3, 10-23. [196] Nayak, T. and Patangray, A. J. (2015). Biofertilizer-beneficial for sustainable agriculture and improving soil fertility. Asian J. Multidisciplinary Studies, 3, 189-194.

42


[197] Raei, Y. and Aghaei-Gharachorlou, P. (2015). Organic cultivation of industrial crops: a review. J. Bio. Env. Sci., 6, 366-377. [198] Burdman, S., Jurkevitch, E. and Okon, Y. (2000). Recent advances in the use of plant growth promoting rhizobacteria (PGPR) in agriculture. In: N. S. S. Rao and Y. R. Dommergues (Eds.), Microbial interactions in agriculture and forestry (pp. 229-250). Enfield, US, Science Publishers. [199] Lucy, M., Reed, E. and Glick, B. R. (2004). Applications of free living plant growth-promoting rhizobacteria. A Van Leeuw, 86, 1-25. [200] Mehnaz, S. (2015). Azospirillum: A biofertilizer for every crop. Plant Microbes Symbiosis: Applied Facets, 297-314. [201] Abd El-Fattah, D. A., Ewedab, W. E., Zayed, M. S. and Hassaneina, M. K. (2013). Effect of carrier materials, sterilization method, and storage temperature on survival and biological activities of Azotobacter chroococcum inoculants. Ann. Agric. Sci., 58, 111-118. [202] Wani, S. A., Chand, S. and Ali, T. (2013). Potential use of Azotobacter chroococcum in crop production: an overview. Curr. Agric. Res. J., 1, 35-38. [203] Adesemoye, A. O., Torbert, H. A. and Kloepper, J. W. (2008). Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can. J. Microbiol., 54, 876-886. [204] Hasnain, S. and Sabri, A. N. (1996). Growth stimulation of Triticum aestivum seedlings under Cr-stress by nonrhizospheric Pseudomonas strains. In: Abstract book of 7th international symposium on nitrogen fixation with non-legumes, Faisalabad, p. 36. [205] Morris, R. O. (1986). Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu. Rev. Plant Physiol., 37, 509-538. [206] Akiyoshi, D. E., Regier, D. A. and Gordon, M. P. (1987). Cytokinin production by Agrobacterium and Pseudomonas spp. J. Bacteriol., 169, 4242-4248. [207] Mutka, A. M., Fawley, S., Tsao, T. and Kunkel, B. N. (2013). Auxin promotes susceptibility to Pseudomonas syringae via a mechanism independent of suppression of salicylic acid-mediated defenses. Plant J., 74, 746-754. [208] Fett, W. F., Osman, S. F. and Dunn, M. F. (1987). Auxin Production by Plant-Pathogenic Pseudomonads and Xanthomonads. Appl. Environ. Microbiol., 53, 1839-1845. [209] Smidt, M. and Kosuge, T. (1978). The role of indole-3-acetic acid accumulation by alpha methyl tryptophan-resistant mutants of


43

Pseudomnonas saivastanoi in gall formation on oleanders. Physiol. Plant Pathol., 13, 203-214. [210] Comai, L., Surico, G. and Kosuge, T. (1982). Relation of plasmid DNA to indoleacetic acid production in different strains of Pseudoinonas svringae pv. saivastanoi. J. Gen. Microbiol., 128, 2157-2163. [211] Surico, G., Lacobellis, N. S. and Sisto, A. (1985). Studies on the role of indole-3-acetic acid and cytokinins in the formation of knots on olive and oleander plants by Pseiidoinonas svringtiae pv. sal'astanoi. Physiol. Plant Pathol., 26, 309-320. [212] Liu, S. T., Perry, K. L., Schardl, C. L. and Kado, C. I. (1982). Agrobacterinin Ti plasmid indoleacetic acid gene is required for crown gall oncogenesis. Proc. Natl. Acad. Sci. US, 79, 2812-2816. [213] Offringa, I. A., Melchers, L. S., Regenburg-Tuink, A. J. G., Costantino, P., Schilperoort, R. A. and Hooykaas, P. J. J. (1986). Complementation of Agrobacterium tumefaciens tumor-inducing aux mutant by genes from the TR-region of the Ri plasmid of Agrobacterium rhizogenes. Proc. Natl. Acad. Sci. US, 83, 6935-6939. [214] Clark, E., Manulis, S., Ophir, Y., Barash, I. and Gafni, Y. (1993). Cloning and characterization of iaaM and iaaH from Erwinia herbicola pathovar gypsophilae. Phytopathology, 83, 234-240. [215] Cooksey, D. A. (1986). Galls of Gypsophila paniculata caused by Erwinia herbicola. Plant Dis., 70, 464-468. [216] Manulis, S., Gafni, Y., Clark, E., Zutra, D., Ophir, Y. and Barash, I. (1991). Identification of a plasmid DNA probe for detection of Erwinia herbicola pathogenic on Gypsophila paniculata. Phytopathology, 81, 5457. [217] Burr, T. J., Katz, B. H., Abawi, G. S. and Crosier, D. C. (1991). Comparison of tumorigenic strains of Erwinia herbicola isolated from table beet with E. h. gypsophila. Plant Dis., 75, 855-858. [218] Groenhagen, U., Baumgartner, R., Bailly, A., Gardiner, A., Eberl, L., Schulz, S., Weisskopf, L. (2013). Production of bioactive volatiles by different Burkholderia ambifaria strains. J. Chem. Ecol., 39, 892-906. [219] Romeo, T., Vakulskas, C. A., Babitzke, P. (2013) Posttranscriptional regulation on a global scale: Form and function of Csr/Rsm systems. Environ. Microbiol., 15, 313-324.

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