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The Scientific World Journal
Volume 2014 (2014), Article ID 810192, 6 pages
Research Article

Effect of Pseudomonas putida on Growth and Anthocyanin Pigment in Two Poinsettia (Euphorbia pulcherrima) Cultivars

1Facultad de Ciencias Agricolas, Universidad Veracruzana, Circuito Universitario Gonzalo Aguirre Beltran S/N, Zona Universitaria, 91090 Xalapa, VER, Mexico
2Centro de Investigaciones Biologicas del Noroeste, Instituto Politecnico Nacional 195, Colonia Playa Palo de Santa Rita, 23090 La Paz, BCS, Mexico
3Universidad de Sonora, Boulevard Luis Encinas y Rosales, Colonia Centro, 23000 Hermosillo, SON, Mexico

Received 10 March 2014; Revised 29 May 2014; Accepted 12 June 2014; Published 3 July 2014

Academic Editor: Ramesh C. Kasana

Copyright © 2014 Ramon Zulueta-Rodriguez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Pseudomonas putida is plant growth promoting rhizobacteria (PGPR) that have the capacity to improve growth in plants. The purpose of this study was to determine growth and anthocyanin pigmentation of the bracts in two poinsettia Euphorbia pulcherrima cultivars (Prestige and Sonora Marble) using three strains of P. putida, as well as a mixture of the three (MIX). Comparison with the control group indicated for the most part that Prestige grew better than the Sonora Marble cultivars with the PGPR strains. Prestige with the MIX strain grew better compared to control for the number of cyathia (83 versus 70.4), volume of roots (45 versus 35 cm3), number of leaves (78 versus 58), and area of leaf (1,788 versus 1,331 cm2), except for the number of flowers (8.8 versus 11.6). To the naked eye, coloration of plants appeared identical in color compared to the control group. For all plants with P. putida strains, there was less anthocyanin pigment, but biomass was always greater with PGPR strains. Nevertheless, to the naked eye, the coloration of the plants appeared identical in color compared to the control group. This is the first study reporting the positive effects of P. putida rhizobacteria treatments on growth of poinsettia cultivars.

1. Introduction

The poinsettia Euphorbia pulcherrima of the family Euphorbiaceae is a member of the spurge family of plants which is made up of 300 genera and around 7,500 species; some have economic importance such as Ricinus communis (castor oil) or Jatropha curcas (biodiesel). The poinsettia is an ornamental plant of economic importance in Mexico, United States, and other countries. The majority of plants are sold in December with preferred colors being red, green, white, and purple colored plants. Red plants are particularly popular with worldwide sales of over $145 million [1].

Mexico is the fourth worldwide, producing an estimated 20 million plants per year with a value of 54 million USD, covering an area of 320 hectares. In cultivation of the poinsettia, it is important to produce plants with intense color foliage for consumer acceptance. The presence of anthocyanin determines the intensity or lack of red color in the bracts [2]. To achieve the color intensity, plant handling involves controlling photoperiod and nutrition. The application of chemical fertilizers can affect negatively nutrition and as a consequence the color in poinsettia plants. Hence, there is a growing interest in looking for options that reduce the use of chemicals to maintain plant health and reduce production costs. Among the options is the use of bacteria whose habitat is located in a zone surrounding the roots of the plants or rhizosphere. These bacteria, appropriately called rhizobacteria, are known as plant growth promoting rhizobacteria (PGPR) [3]. PGPR produce physiologically active substances that encourage seed germination, host growth acceleration, and increase crop yield, improving plant defenses against pathogens [4, 5]. Rhizobacteria have played an important role in moderating the excessive use of fertilizers and pesticides [6, 7].

PGPR within genera known to stimulate the growth of plants are Azospirillum, Azotobacter, Bacillus, Enterobacter, and Pseudomonas. The latter has been studied in recent years for its beneficial effects when used as organic fertilizer or as agents for biological control of pathogens [8]. One outstanding species is Pseudomonas putida, which is considered a metabolically versatile rhizobacterium ideal for agriculture applications. P. putida is known to quickly colonize the rhizosphere of plants thus outcompeting plant pathogens [9]. Despite the benefits found in various plants of agricultural interest [10], these rhizobacteria have not been evaluated thus far in poinsettia plants.

Among the few studies of rhizobacteria in ornamental plants is that of van Peer et al. [11] where they found that WCS417r strain of P. fluorescens protects carnation (Dianthus caryophyllus L.) plants against Fusarium oxysporum. Along the same lines of biological control, Shanmugam et al. [12] reported that Bacillus atrophaeus and Burkholderia cepacia substantially inhibit the development of F. oxysporum in gladiolus (Gladiolus hortulanus L. H. Bailey). In terms of improving growth, Sivakumar et al. [13] reported that inoculation of geranium (Pelargonium graveolens) with P. fluorescens enhances growth and biomass. Similarly, Padmadevi et al. [14] reported that the application of Azospirillum sp. and phosphate solubilizing bacteria (phosphobacteria) improves floral attributes (Anthurium andreanum Lind.) and that of Ambrosini et al. [15] where they reported that the genera Burkholderia, Achromobacter, Chryseobacterium, and Azospirillum had a stimulatory effect on plant growth of the sunflower (Helianthus annuus L.).

Poinsettia is a valuable ornamental plant with a short window of extraordinary commercial demand and sales during the month of December. To supply this demand peak, it is essential to have plants available within a short temporal space with their respective coloration. It is known in other plants that rhizobacteria microorganisms promote growth. Therefore, the purpose of this study was to determine the effect of three strains of Pseudomonas putida on growth and anthocyanin pigmentation in the bracts of two poinsettia cultivars.

2. Materials and Methods

2.1. Experimental Study Site

The experiment was conducted in a nursery located in La Estanzuela, Veracruz, Mexico, km. 5.5, Road Las Trancas-Coatepec, municipality of Emiliano Zapata (19°N, 96°W).

2.2. Bacterial Inoculum Preparation

We used three strains of P. putida labeled as FCA-8, FCA-56, and FCA-60 and prepared one MIX strain by mixing 20 mL of each of the three strains. These strains were originally isolated from Citrus volkameriana Tan. & Pasq. and provided by the Laboratorio de Quimica, Facultad de Ciencias Agricolas, Universidad Veracruzana, Xalapa, Veracruz, Mexico. All rhizobacteria were grown in King’s B medium (glycerol 10 mL, protease-peptone 20 g, 1.5 g, K2HPO4 1.5 g, agar 15 g, and sterile distilled water 1 L) at 28°C for 24 h. For all strains including MIX, the bacterial concentration was adjusted to 109 cells  using a digital spectrometer Thermo Spectronic Genesys 20 (Thermo Electron Scientific Instruments Corp., Madison, WI) at a wavelength of 660 nanometers (nm) and absorbance of 1.

2.3. Vegetative Material Preparation

Cuttings were obtained of poinsettia Prestige and Sonora Marble cultivars from the International Poinsettia Nursery S.A. de C.V., located in Cuernavaca, Morelos, Mexico. The cuttings obtained for the two cultivars were 8 cm tall with 7 leaves. The substrate used consisted of pine sapwood (68%), tepezil (23%), and sand (9%) and was disinfected with 100 mL  of metam sodium (the third most commonly used agricultural pesticide in the USA). Pots of rigid polyethylene of 14 cm in diameter and with a height of 10.5 cm were filled with 500 g of the prepared substrate and one transplanted cutting was placed per container.

2.4. Experimental Inoculation

The roots of the cuttings of eight separate groups of seedlings of poinsettia Prestige and Sonora Marble cultivars (4 groups of each cultivar) were inoculated immediately at transplant with a single application of individual rhizobacteria strains FCA-8, FCA-56, FCA-60, and MIX by placing 2  of the bacterial suspension directly to root before covering it with a soil mixture. A ninth group (control) only received fertilizer and water. All cuttings were fertilized with the recommended commercial dose every 15 days with 0.75 g L−1 of NO3 : P2O5 : K2O (15–05–25), 100 mg  of calcium nitrate, 60 mg L−1 of micronutrients, and 0.05 mL L−1 of molybdenum. All cuttings were watered daily.

At 110 days after inoculation (DAI) the following was quantified: plant height (cm), stem diameter (mm), leaf area (cm2), number of cyathia, flowers, secondary stems, bracts and leaves, volume root (cm3), area of bracts (modified leaves red for Prestige and yellow for Sonora Marble cultivars, in units of cm2), fresh and dry biomass of bracts, leaves, stems, and roots. Ten replicates were used per treatment and the experiment was repeated twice.

2.5. Extraction of Anthocyanin

The anthocyanin pigments were extracted by macerating poinsettia bracts in water and filtering the mixture. Anthocyanin extraction was conducted with acidified methanol with 0.1 M HCl (85 : 15, v/v) [16, 17]. Once the anthocyanin sample was eluted, it was analyzed immediately so that the pigment would not degrade. This was carried out by diluting the sample and taking the spectral measurement.

2.6. Spectral Measurement of the Relative Anthocyanin Content in Bracts

The absorbance which is related to concentration of red pigment anthocyanin in poinsettia bracts was measured at of 547 nm at pH 1 [18]. The reference blank contained only acidified methanol with 0.1 M HCl (85 : 15, v/v). For all spectral measurements, a spectrophotometer Thermo Spectronic Genesys 20 (Thermo Electron Scientific Instruments Corp., Madison, WI) was used. A total of 10 bracts were analyzed per treatment and the experiment was repeated twice.

2.7. Colonization Rhizobacteria

The total population of the Pseudomonas strains was determined at 110 DAI of cuttings by dilution technique on plate count following the methodology proposed by Holguin and Bashan [19]. A composite sample of roots of 1.5 g was collected following each treatment; it was macerated and dilutions were made in glass test tubes with 0.85% NaCl. The obtained dilutions were inoculated into a medium of cetrimide agar plates supplemented with 2 ppm of fluconazole which inhibits growth of filamentous fungi and incubated at 28°C for 72 h. Rhizobacterium population of each was expressed in colony forming units (CFU, ). There were three replicates per treatment and the experiment was repeated twice.

2.8. Statistical Analysis

The data were processed by one-way analysis of variance (ANOVA). We used the statistical package Statistica v. 10.0 for Windows (StatSoft) and post hoc Tukey’s test () was used for comparison of means.

3. Results and Discussion

The inoculation with different strains of Pseudomonas putida was found to have an influence on the growth and anthocyanin pigment contents of the bracts of poinsettia plants. The differences in growth parameters which included number of cyathia, number of flowers, volume of roots, number of leaves, area of leaf, fresh biomass of leaves and bracts, and area of bracts varied depending on the cultivar (Prestige and Sonora Marble) and strain of rhizobacteria in comparison to the control (not inoculated with rhizobacteria). Of the two cultivars, Prestige had a better response in terms of growth variables with the rhizobacteria.

For example, considering only Prestige (Table 1), the number of cyathia and flowers was greatest for FCA-60, root volume for MIX, number of leaves for FCA-56 and MIX, area of the leaf for FCA-8, FCA-56, and MIX, fresh biomass of leaves for FCA-60 and MIX and bracts for MIX, and area of bracts for FCA-8, FCA-60, and MIX. For Prestige, overall best strains for promoting growth and development compared to the control were in general F-60 and MIX. Strain FCA-60 promoted higher values for cyathia (36%), flowers (37%), and fresh biomass of leaves (22%) (Tables 1 and 2). All other growth parameters using F-60 with Prestige were not significantly different (). The inoculation with the three strains of P. putida (MIX) in Prestige increased the number of cyathia (17%), root volume (27%), number of leaves (35%), and area of leaf (34%) and had more fresh biomass of leaves (26%) and bracts (31%). For the MIX strain of Prestige only two growth parameters were not significantly different (); these were number of flowers and area of bracts.

Table 1: Effects of Pseudomonas putida strains on growth promotion of poinsettia Prestige and Sonora Marble cultivars.
Table 2: Effects of Pseudomonas putida strains on growth promotion of poinsettia Prestige cultivar.

For Sonora Marble, the growth parameters measured with the P. putida strains were not significantly different () and for the majority of the strains were lower than the control. For Sonora Marble (Table 1), the number of cyathia was the greatest for control. For number of flowers and volume of root, the MIX and FCA-8 strains were the best, respectively. For number of leaves, the MIX and FCA-56 were the best. Sonora Marble did not show significant differences in bract area and fresh biomass (hence, data not shown), while Prestige did show differences of fresh biomass of leaves and bracts depending on the strain P. putida (Table 2). For Sonora Marble, the best strain for growth was the mixture of the three (MIX); individual strains generally did not improve growth parameters when compared to control (no rhizobacteria). The MIX strain in Sonora Marble increased the number of flowers (28%) and number of leaves (1.7%). However, the MIX strain also had lower values in other growth parameters such as for number of cyathia (8%), volume of roots (23%), and area of leaf (3.7%) in comparison with control.

The rhizobacteria apparently increased the capacity of absorption of nutrients and water in the roots of plants [20, 21] probably from the fertilization treatments. This has been shown to be the case in various cereals. In these studies, it has been found that by simultaneously applying nitrogen and phosphorus with rhizobacteria it was possible to improve growth, yield, and quality of grain [22]. Furthermore, the positive response of the plants due to the inoculation of the different strains of P. putida for both cultivars and in particular Prestige may be due to a hormonal effect of the rhizobacteria, whether it is being produced directly via an auxin and/or gibberellin [23]. These provide metabolizing signaling compounds that directly affect the regulation production of plant hormones [24, 25]. One of the main effects of this altered phytohormone production is a more elongated and nested root structure. Increased root volume allows for soil exploration improving water capture and nutrient assimilation [26]. However, it is important to note that the mechanism described above for P. putida is not the only possible explanation for plant growth. Another possibility could be related to its ability to better solubilize P, which can lead to a production of a wide variety of antimicrobial metabolites including enzymes, siderophores, volatile compounds, cyclic lipopeptides (CLPs), and antibiotics [27, 28].

Even though the strains of P. putida have a positive effect on plant growth in our experiment, Sonora Marble did not show a positive response in most of its other variables. This effect is possibly due to low P. putida colonization in the root of this cultivar (Figure 1), which was less compared to the other cultivars. For both Prestige and Sonora Marble cultivars, control groups without P. putida had 0 CFU colonization, indicating that there was no contamination with other bacteria (data not shown). One possibility for this behavior is that the Sonora Marble possibly exudates compounds in its roots which limit colonization of different strains of P. putida [29, 30]. In plants such as tomato, the colonization of the roots for rhizobacteria depends on a great variety of chemical compounds such as succinic acid, malic acid, L-aspartic, L-glutamic acid, L-isoleucine, L-leucine, and L-lysine [31]. It has been reported that Prestige exudates compounds in the root which are favorable for colonization [32]. Hence, in Prestige the establishment of its rhizosphere was probably aided by root exudates that favored P. putida colonization [33, 34]. Nevertheless, literature searches revealed no information about the type or amount of compounds in poinsettias exudates with rhizobacteria.

Figure 1: Population of Pseudomonas putida strains in the rhizosphere of poinsettia Prestige and Sonora Marble cultivars. Colony forming units (CFU) in plants with P. putida strain: FCA-8, FCA-56, FCA-60, and MIX (inoculated simultaneously with the three rhizobacteria) at 110 DAI. Data for controls of both Prestige and Sonora Marble cultivars are not shown since they were found to have 0 CFU.

In regard to anthocyanin, it was found that in Prestige (red bracts) the absorbance was approximately two times higher than for Sonora Marble (yellow bracts), indicating that anthocyanin amount is lower in this cultivar (Table 3). Also found was that among the cultivar treatments the amount of anthocyanin varied very little compared to the control. This was corroborated by visual inspection since all treatments had the same characteristic color as the control.

Table 3: Effects of Pseudomonas putida strains on the anthocyanin pigment contents of the bracts of poinsettia plants.

4. Conclusion

As far as the authors are aware, this is the first report of inoculation of poinsettia (Euphorbia pulcherrima) plants with different strains of Pseudomonas putida, plant growth promoting rhizobacteria (PGPR). The highlight of this study is that the PGPR used in this study improved some growth parameters in two poinsettia cultivars (Prestige and Sonora Marble) and did not deteriorate poinsettia color. In terms of growth and developmental parameters, it was found that Prestige responded better to the individual strains of P. putida than Sonora Marble; possibly causes are root exudates that favored particular strains of PGPR more so in Prestige. In general, the data of this study also suggests that certain strains of P. putida can in particular cultivars of poinsettia improve growth parameters, but not in all. The long term perspective is to determine if P. putida will allow for reduction of fertilizer when growing poinsettia thus possibly allowing for improvement of production costs. It is also important to point out that this study, which identifies improvements in growth with P. putida rhizobacteria, is required before any detailed studies of mechanism(s) are undertaken. Studies of mechanism(s) are beyond the scope of the present study. However, having said this, it is important to point out that indeed future work will involve not only reduction of fertilizer, but also studies of the mechanism(s) of growth such as identifying growth hormones (such as IAA, gibberellic acid), determining P-solubilization and siderophore production.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.


  1. US Department of Agriculture, Floriculture Crops 2010 Summary, National Agricultural Statistics Service, Washington, DC, USA, 2011.
  2. M. D. Bennett, H. J. Price, and J. S. Johnston, “Anthocyanin inhibits propidium iodide DNA fluorescence in Euphorbia pulcherrima: implications for genome size variation and flow cytometry,” Annals of Botany, vol. 101, no. 6, pp. 777–790, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. J. W. Kloepper and M. N. Schroth, “Plant growth promoting rhizobacteria on radishes,” in Proceedings of the 4th International Conference on Plant Pathogenic Bacteria, pp. 879–882, INRA, Angers, France, 1978.
  4. G. Lazarovits, “Application of growth-promoting rhizobacteria to transplant plug and seed,” HortScience, vol. 30, no. 4, p. 750, 1995. View at Google Scholar
  5. B. S. Saharan and V. Nehra, “Plant growth promoting rhizobacteria: a critical review,” Life Sciences and Medicine Research, vol. 21, pp. 1–30, 2011. View at Google Scholar
  6. M. Ashrafuzzaman, F. A. Hossen, M. R. Ismail et al., “Efficiency of plant growth-promoting rhizobacteria (PGPR) for the enhancement of rice growth,” African Journal of Biotechnology, vol. 8, no. 7, pp. 1247–1252, 2009. View at Google Scholar · View at Scopus
  7. R. K. Mishra, O. Prakash, M. Alam, and A. Dikshit, “Influence of plant growth promoting rhizobacteria (PGPR) on the productivity of Pelargonium graveolens L Herit,” Recent Research in Science and Technology, vol. 2, no. 5, pp. 53–57, 2010. View at Google Scholar
  8. B. Lugtenberg and F. Kamilova, “Plant-growth-promoting rhizobacteria,” Annual Review of Microbiology, vol. 63, pp. 541–556, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. M. N. Hassan, S. Afghan, and F. Y. Hafeez, “Biological control of red rot in sugarcane by native pyoluteorin-producing Pseudomonas putida strain NH-50 under field conditions and its potential modes of action,” Pest Management Science, vol. 67, no. 9, pp. 1147–1154, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. Z. Cheng, O. Z. Woody, B. J. McConkey, and B. R. Glick, “Combined effects of the plant growth-promoting bacterium Pseudomonas putida UW4 and salinity stress on the Brassica napus proteome,” Applied Soil Ecology, vol. 61, pp. 255–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. R. van Peer, G. J. Niemann, and B. Schippers, “Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r,” Phytopathology, vol. 81, no. 7, pp. 728–734, 1991. View at Google Scholar · View at Scopus
  12. V. Shanmugam, N. Kanoujia, M. Singh, S. Singh, and R. Prasad, “Biocontrol of vascular wilt and corm rot of gladiolus caused by Fusarium oxysporum f. sp. gladioli using plant growth promoting rhizobacterial mixture,” Crop Protection, vol. 30, no. 7, pp. 807–813, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. B. S. Sivakumar, N. Earanna, A. A. Farooqi, D. J. Bagyaraj, and C. K. Suresh, “Effect of AM fungus and plant growth promoting rhizomicroorganisms (PGPRs) on growth and biomass of geranium (Pelargonium graveolens),” Journal of Soil Biology and Ecology, vol. 22, pp. 27–30, 2002. View at Google Scholar
  14. K. Padmadevi, M. Jawaharlal, and M. Vijayakumar, “Effect of biofertilizers on floral characters and vase life of anthurium (Anthurium andreanum Lind.) cv. Temptation,” South Indian Horticulture, vol. 52, no. 1–6, pp. 228–231, 2004. View at Google Scholar
  15. A. Ambrosini, A. Beneduzi, T. Stefanski, F. G. Pinheiro, L. K. Vargas, and L. M. P. Passaglia, “Screening of plant growth promoting rhizobacteria isolated from sunflower (Helianthus annuus L.),” Plant and Soil, vol. 356, no. 1-2, pp. 245–264, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. H. W. Siegelman and S. B. Hendricks, “Plant photocontrol of anthocyanin synthesis in apple skin,” Plant Physiology, vol. 33, no. 3, pp. 185–190, 1958. View at Publisher · View at Google Scholar
  17. M. K. Kim, H. A. Kim, K. Koh, H. S. Kim, and Y. S. Lee, “Identification and quantification of anthocyanin pigments in colored rice,” Nutrition Research and Practice, vol. 2, no. 1, pp. 46–49, 2008. View at Publisher · View at Google Scholar
  18. T. Fuleki and F. J. Francis, “Quantitative methods for anthocyanins: extraction and determination of total anthocyanin in cranberries,” Journal of Food Science, vol. 33, no. 1, pp. 72–77, 1968. View at Google Scholar
  19. G. Holguin and Y. Bashan, “Nitrogen-fixation by Azospirillum brasilense CD is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.),” Soil Biology and Biochemistry, vol. 28, no. 12, pp. 1651–1660, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Yildirim, H. Karlidag, M. Turan, A. Dursun, and F. Goktepe, “Growth, nutrient uptake, and yieldpromotion of broccoli by plantgrowth promoting rhizobacteriawith manure,” HortScience, vol. 46, no. 6, pp. 932–936, 2011. View at Google Scholar · View at Scopus
  21. M. Yasin, K. Ahmad, W. Mussarat, and A. Tanveer, “Bio-fertilizers, substitution of synthetic fertilizers in cereals for leveraging agriculture,” Crop and Environment, vol. 3, pp. 62–66, 2012. View at Google Scholar
  22. V. Kumar, R. K. Behl, and N. Narula, “Effect of phosphate-solubilizing strains of azotobacter chroococcum on yield traits and their survival in the rhizosphere of wheat genotypes under field conditions,” Acta Agronomica Hungarica, vol. 49, no. 2, pp. 141–149, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. L.-X. Yao, Z.-S. Wu, Y.-Y. Zheng, I. Kaleem, and C. Li, “Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton,” European Journal of Soil Biology, vol. 46, no. 1, pp. 49–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. W. T. Frankenberger and M. Arshad, Phytohormones in Soils: Production and Function, Marcel Dekker, New York, NY, USA, 1995.
  25. R. J. Ryu and C. L. Patten, “Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5,” Journal of Bacteriology, vol. 190, no. 21, pp. 7200–7208, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. I. C. Dodd, N. Y. Zinovkina, V. I. Safronova, and A. A. Belimov, “Rhizobacterial mediation of plant hormone status,” Annals of Applied Biology, vol. 157, no. 3, pp. 361–379, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Dey, K. K. Pal, D. M. Bhatt, and S. M. Chauhan, “Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria,” Microbiological Research, vol. 159, no. 4, pp. 371–394, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Ahmad, I. Ahmad, and M. S. Khan, “Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities,” Microbiological Research, vol. 163, no. 2, pp. 173–181, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. L. L. McCarter, “Dual flagellar systems enable motility under different circumstances,” Journal of Molecular Microbiology and Biotechnology, vol. 7, no. 1-2, pp. 18–29, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. O. V. Mavrodi, D. V. Mavrodi, A. A. Park, D. M. Weller, and L. S. Thomashow, “The role of dsbA in colonization of the wheat rhizosphere by Pseudomonas flourescens Q8r1-96,” Microbiology, vol. 152, no. 3, pp. 863–872, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. S. de Weert, I. Kuiper, E. L. Lagendijk, G. E. M. Lamers, and B. J. J. Lugtenberg, “Role of chemotaxis toward fusaric acid in colonization of hyphae of Fusarium oxysporum f. sp. radicis-lycopersici by Pseudomonas fluorescens WCS365,” Molecular Plant Microbe Interactions, vol. 17, no. 11, pp. 1185–1191, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. A. B. Herman, B. A. Nault, and C. D. Smart, “Effects of plant growth-promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York,” Crop Protection, vol. 27, no. 6, pp. 996–1002, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Benizri, E. Baudoin, and A. Guckert, “Root colonization by inoculated plant growth-promoting rhizobacteria,” Biocontrol Science and Technology, vol. 11, no. 5, pp. 557–574, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Dutta and A. R. Podile, “Plant Growth Promoting Rhizobacteria (PGPR): the bugs to debug the root zone,” Critical Reviews in Microbiology, vol. 36, no. 3, pp. 232–244, 2010. View at Publisher · View at Google Scholar · View at Scopus