Subscribe Now Subscribe Today
Abstract
Fulltext PDF
References
Research Article
 

Interaction Between Pseudomonas fluorescens FPD-15 and Bradyrhizobium spp. in Peanut



A. Vikram, H. Hamzehzarghani, K.I. Al-Mughrabi, P.U. Krishnaraj and K.S. Jagadeesh
 
ABSTRACT

In this study the ability of Pseudomonas fluorescens FPD-15 to promote plant growth was assessed under greenhouse conditions using JL-24 variety of peanut as a test crop. A pot experiment was carried out in completely randomized factorial design with two main factors to investigate the effect of application of Pseudomonas fluorescens FPD-15 with Bradyrhizobium strains NC-92 and SSP-24 under preincubated and coinoculated conditions (as a main factor with seven levels) at different time intervals (as the second main factor with three levels) with 3 replicates. Analysis of Variance (ANOVA) on each measured response variable (comprising root and shoot biomass, nodule number and dry weight and nitrogen content) was performed using the GLM procedure of SAS. The inoculation of peanut seeds with FPD-15 significantly increased root and shoot dry weight, nodule number and dry weight and N content in shoot when compared to the control. The interaction between FPD-15 and Bradyrhizobium strains NC-92 and SSP-24 were studied under preincubated and coinoculated conditions. The preincubated treatments yielded significantly higher root and shoot dry weight, nodule number, nodule dry weight and percent N content of shoot compared to the coinoculated treatments. Field trials using these strains should be conducted before they can be exploited in a commercial set up.

Services
Related Articles in ASCI
Similar Articles in this Journal
Search in Google Scholar
View Citation
Report Citation

 
  How to cite this article:

A. Vikram, H. Hamzehzarghani, K.I. Al-Mughrabi, P.U. Krishnaraj and K.S. Jagadeesh, 2007. Interaction Between Pseudomonas fluorescens FPD-15 and Bradyrhizobium spp. in Peanut. Biotechnology, 6: 292-298.

DOI: 10.3923/biotech.2007.292.298

URL: https://scialert.net/abstract/?doi=biotech.2007.292.298

INTRODUCTION

The rhizosphere bacteria that aggressively colonize roots were termed as rhizobacteria. The term plant growth Promoting Rhizobacteria (PGPR) was coined by Kloepper et al. (1980) to include bacteria inhabiting the root and rhizosphere and having the ability to increase plant growth. These microorganisms have the ability to aggressively colonize plant roots and stimulate growth of plants in addition to suppressing plant pathogens (Kloepper et al., 1999; Weller et al., 2002; Pieterse et al., 2002; Vessey, 2003; Lucy et al., 2004; Preston, 2004). The beneficial effects of PGPR are attributed to improvement of plant growth and health and can be evidenced by an increase in seedling emergence, vigor, root system development and yield. The possible mechanisms by which PGPR increase the yield of crops include biocontrol of phytopathogenic fungi, hormone production and increased uptake of nutrients such as N, P and K (Kapulnik et al., 1985; Lifshitz et al., 1987; Defreitas and Germida, 1990b; Kloepper, 1993). PGPR, such as fluorescent pseudomonads, have been used as seed inoculants to promote plant growth and increase yields (Kloepper et al., 1980; Defreitas and Germida, 1990a). Positive effects of PGPR on diverse hosts such as bean (Anderson and Guera, 1985), cotton (Sakthivel et al., 1986), soybean (Polonenko et al., 1987), peanut (Dey et al., 2004), maize (Shaharoona et al., 2006) and sugarbeet (Cakmakci et al., 2006) are common in literature. A review published recently by Gray and Smith (2005) dealt with the history of PGPR discovery and indicated the progress in understanding each of the PGPR groups. However, PGPR has not yet been fully exploited in Karnataka region and studies on the interaction of Pseudomonas fluorescens with Bradyrhizobium are meager. The present study deals with the effect of Pseudomonas fluorescens FPD-15 alone or in combination with Bradyrhizobium sp. on promoting growth of peanut.

MATERIALS AND METHODS

Greenhouse evaluation of bacterial strains: A pot experiment was conducted under greenhouse conditions at the Department of Agricultural Microbiology, UAS, Dharwad using peanut (variety JL-24) as a test crop. The experiment was conducted in pots (15x15 cm) set in a factorial design which was completely randomized. The soil used in the study was medium black clay obtained from E-block, Main Research Station, UAS Dharwad, India. The peanut seeds were sown after bacterizing them with respective treatments containing bacterial cultures. In the beginning two seeds were planted in each pot and after germination only one seedling was retained. All the pots were maintained in the greenhouse up to a period of 49 days. The plants were sampled at 35, 42 and 49 days after inoculation and were used for analysis. Each pot comprised of an experimental unit and the treatments (inoculationxtime) were assigned randomly to the pots. The trial consisted of treatments (with 8 levels) and days after inoculation (independent pots with 3 levels of 35, 42 and 49 Days After Inoculation (DAI)) as two main factors with eight treatments replicated three times. The treatment combinations were: 1) Uninoculated control; 2) Pseudomonas fluorescens FPD-15 single inoculation; 3) Bradyrhizobium sp. NC-92 single inoculation; 4) Bradyrhizobium sp. SSP-24 single inoculation; 5) Pseudomonas fluorescens FPD-15 + Bradyrhizobium sp. NC-92 preincubated; 6) Pseudomonas fluorescens FPD- 15 + Bradyrhizobium sp. SSP-24 preincubated; 7) Pseudomonas fluorescens FPD-15 + Bradyrhizobium sp. NC-92 coinoculated; and 8) Pseudomonas fluorescens FPD-15 + Bradyrhizobium sp. SSP-24 coinoculated.

The population of Pseudomonas fluorescens FPD-15, Bradyrhizobium sp. NC-92 and Bradyrhizobium sp. SSP-24 at the time of sowing was 8.2x108, 6.2x108 and 6.5x108 cfu mL-1, respectively. The interaction between Pseudomonas fluorescens FPD-15 and strains of Bradyrhizobium sp. were studied in two ways. In one set called preincubation, equal suspensions of both bacteria were mixed and incubated together for five hours on a rotary shaker at 50 rpm and 28°C as per the protocol of Nishijima et al. (1988) and then used for inoculation. For coinoculation, the individually grown cultures were mixed in equal proportions just before sowing and were then applied. In both preincubated and coinoculated treatments, the seeds were bacterized with one mL of bacterial suspension. Bacterial cultures used in the present study were obtained from the Department of Agricultural Microbiology, UAS, Dharwad, India. The root and shoot dry weights were estimated after drying in an oven at 65°C till constant weight and N content in shoot was determined by Kjeldahl method (Jackson, 1973).

Statistical analysis: The statistical model was factorial with a completely randomized design. Treatment with 7 levels and Days after Inoculation (DAI) were considered as main effects and their effects on response variables (root and shoot dry weight, nodule number, nodule dry weight and nitrogen content) were analyzed using General Linear Model (GLM) procedure of SAS (SAS Institute, 1999). Data matrix comprised a data set of the differences between each observation and its un-inoculated control. Multiple comparisons of individual means were performed by Duncan’s multiple range test and using mean statement in the GLM procedure.

RESULTS

The effect of both main factors (treatment and time) was highly significant (p<0.001) on all response variables investigated in this study (Table 1). The highest root dry weights were observed by NC-92 single inoculation and FPD-15 + NC-92 preincubated treatments at 49 DAI. Root dry weights at 49 DAI were also significantly (p<0.05) higher than those at 35 and 42 DAI (Fig. 1a). Inoculation with FPD-15 significantly improved the dry matter accumulation in shoot at 49 DAI over others at all stages of growth. Compared to all stages of growth, the preincubated treatments recorded significantly (p<0.05) higher shoot dry weight than their coinoculated counterparts and highest shoot dry weight was observed due to inoculation of preincubated treatment with FPD-15 and NC-92. The treatments FPD-15 + NC-92 preincubated, FPD-15 + SSP-24 preincubated and FPD-15 + NC-92 coinoculated at 49 DAI produced the first, second and third significantly (p<0.05) highest shoot dry weights, respectively (Fig. 1b).

The treatment involving inoculation with Pseudomonas fluorescens FPD-15 recorded significantly (p<0.05) higher nodule number and dry weight at 49 DAI than other stages of growth, whereas it had no effect on nitrogen content over time (Fig. 1c-e). The preincubated treatments recorded significantly (p<0.05) higher nodule number and dry weights than the coinoculated treatments. Highest nodule number and dry weight was for the preincubated treatment inoculated with FPD-15 and NC-92, followed by FPD-15 and SSP-24 (Fig. 1c and d). At 35, 42 and 49 DAI, the preincubated treatments were statistically significant over coinoculated treatments with regard to the percent of N content in shoot of peanut plants and generally fewer treatments showed significant change in N content over time (Fig. 1e).

Table 1: Factorial analysis of variance of root dry weight, shoot dry weight, nodule number, nodule dry weight and nitrogen content in peanut plants inoculated with Pseudomonas fluorescens and strains of Bradyrhizobium
Results in terms of significance probabilities (P>F). There were 7 treatments (Treat) and 3 Days after Inoculation (DAI) as main effects and the interaction between the main effects (Treat*DAI) were also tested

Fig. 1: Mean profiles of a) root dry weight, b) shoot dry weight, c) nodule number, d) nodule dry weight and e) nitrogen content over a period of 14 days after inoculation. The comparison of mean are done using Duncan’s Multiple Range test at p<0.05 and bars with same letter are not significantly different. Means are deducted from un-inoculated control, T1 = FPD-15 single inoculation, T2 = NC- 92 single inoculation, T3 = SSP-24 single inoculation, T4 = FPD-15 + NC-92 preincubated, T5 = FPD-15 + SSP-24 preincubated, T6 = FPD-15 + NC-92 coinoculated and T7 = FPD-15 + SSP-24 coinoculated; D35, D42 and D49 = 35, 42 and 49 days after inoculation

DISCUSSION

Plant Growth Promoting Rhizobacteria (PGPR) competitively colonize plant roots, stimulate plant growth and reduce the incidence of plant diseases. Fluorescent pseudomonads are a group of PGPRs which have also been responsible for improving the overall growth of many crops (Wang et al., 2000; Dey et al., 2004). In the present investigation, the effect of inoculation of FPD-15 to improve root growth, shoot growth, nodulation and N uptake in peanut plants was assessed. The interaction effects of Pseudomonas fluorescens FPD-15 and strains of Bradyrhizobium were also studied. Inoculation of FPD-15 was found to have a positive effect on improving root biomass, shoot growth, nodulation and shoot N concentration. Increased root and shoot growth could be attributed to the ability of this strain to solubilize phosphate and to release growth promoting substances such as auxins and cytokinins. The inoculation of mineral phosphate solubilizing bacteria increased the total biomass and grain yield in chickpea (Alagawadi and Gaur, 1988) and other leguminous crops (Gaur, 1990). The role of phytohormones such as auxins and cytokinins in enhancing plant cell division and root development is well known (Arshad and Frankenberger Jr., 1993). Pseudomonas fluorescens improved plant growth through the production of growth promoting substances such as indole acetic acid (Dey et al., 2004) and cytokinins (Neito and Frankenberger, 1989). Plant growth promotion observed in agronomic crops due to inoculation of rhizobacteria could be attributed to the increase in nitrogen fixation, production of growth hormones, solubilization of phosphates, oxidation of sulphur, increase in nitrate availability, extra cellular production of antibiotics, lytic enzymes, hydrocyanic acid, increase in root permeability, competition for available nutrients and root sites and induction of plant systemic resistance (Chanway et al., 1991; Kloepper, 1993; Enebak et al., 1998). It is also suggested that a combination of a few of the probable mechanisms may be operative for any particular PGPR strain (Chakraborty et al., 2006). Thus, the improvement in the characters under study may be attributed to the growth promoting substances produced by between test organism as well as enhanced P availability in the rhizosphere.

Another parameter that influences shoot growth in legumes is N2 fixation. The inoculation with FPD-15 significantly increased nodule number. Exopolysaccharides are known to influence legume root infection and nodulation (Chen et al., 1985; Leigh et al., 1988). FPD-15 was capable of producing exopolysaccharides in the form of slimy growth and also solubilized P when grown on hydroxy apatite medium. It is suggested that the release of such exopolysaccharides might have resulted in noticeable increase in nodulation. The shoot N concentration was also significantly higher in FPD-15 inoculated plants. In leguminous oilseeds, increased nodule number results in increased N fixation and N uptake (Joshi et al., 1990). Inoculation of FPD-15 with NC-92 and SSP-24 both by addition of preincubated mixture or coinoculation, significantly improved the percentage of N accumulated over the respective NC-92 and SSP-24 single inoculations indicating an overall net positive effect of both strains on N uptake. Positive interactions of Pseudomonas fluorescens and Bradyrhizobium have been reported in soybean and chickpea (Polonenko et al., 1987; Alagawadi and Gaur, 1988). Coinoculation of Bacillus polymyxa and Rhizobium etli stimulated Rhizobium etli populations and nodulation in the rhizosphere of Phaseolus vulgaris (Petersen et al., 1996).

Studies involving preincubation of Bradyrhizobium japonicum with Pseudomonas fluorescens increased the level of nodulation in soybean (Nishijima et al., 1988). Hence, the differences between inoculation of preincubated mixture and coinoculation of Pseudomonas fluorescens FPD-15 with Bradyrhizobium strains on growth parameters of peanut was assessed in this trial. While comparing both preincubated and coinoculated treatments it was noted that preincubated treatments had a significantly higher impact on the plant biomass, nodule dry weight and N content in shoot over coinoculation. Preincubation of P. fluorescens and Bradyrhizobium strains significantly increased nodulation over coinoculated treatments. Results of enhanced levels of nodulation were recorded when soybean was treated with Bradyrhizobium japonicum and Pseudomonas fluorescens (Nishijima et al., 1988). They were of the opinion that the enhanced nodulation observed in soybean by Bradyrhizobium japonicum in presence of Pseudomonas fluorescens could be due to a substance produced by Pseudomonas fluorescens SSJ2. Interaction between Bradyrhizobium and plant growth promoting rhizobacteria increased nodulation and nitrogen fixation in soybean and Lupinus albus (Dashti et al., 1998; Garcia et al., 2004). Pseudomonas fluorescens F113 enhanced nodulation by Rhizobium leguminosarum 1112 fourfold in pea plants when they were inoculated after mixing them together (Andrade et al., 1998). The nodules obtained were much larger and strongly pigmented compared to single inoculation of R. leguminosarum 1112. In chickpea, coinoculation of fluorescent Pseudomonas and effective strains of Rhizobium resulted in a significant increase in nodule weight, root and shoot biomass and total plant nitrogen in sterilized chillum jars or under pot culture conditions (Parmar and Dadarwal, 1999). Coinoculation of Bradyrhizobium japonicum USDA 110 with rhizobacterial strains increased nodule number and dry weight of B. japonicum USDA 110 when compared to their single inoculations (Polonenko et al., 1987). These rhizobacteria can promote plant growth indirectly by affecting symbiotic N2 fixation, nodulation, or nodule occupancy. The fact that inoculation of FPD-15 alone or in combination with Bradyrhizobium spp. increased nodulation and N2 fixation than individual inoculation of Bradyrhizobium in the present study could be attributed to two possible reasons. One reason for this observation may be that FPD-15 produced some growth promoting substances which aided in improved nodulation and N2 fixation by Bradyrhizobium. The second reason may be that FPD-15 strain has the capability to fix nitrogen. In studies which were conducted earlier, Pseudomonas fluorescens and Pseudomonas sp. have been shown to fix nitrogen (Gowda and Watanabe, 1985; Chan et al., 1994). However, there are suggestions that the contribution of bacterially fixed nitrogen to plants is minimal and that enhanced growth by an inoculated plant does not necessarily mean that the bacteria associated with the roots do fix nitrogen or pass the products of nitrogen fixation to the plant (James and Olivares, 1997). There are also reports that although PGPR have the ability to fix atmospheric nitrogen, they are not likely to provide large amounts of this fixed nitrogen to the plants (Mantelin and Touraine, 2004). The possible answers to the above could all be answered if acetylene reduction assay of the strain, in vitro nitrogen fixation and refined plant N uptake analysis are conducted. It is suggested that it would be appropriate to test if FPD-15 has the capability to produce growth promoting substances. The ability of Pseudomonas fluorescens FPD-15, alone or in combination with Bradyrhizobium, to promote plant growth in peanut can be commercially exploited only after conducting suitable field trials.

ACKNOWLEDGMENT

The authors would like to thank KSDA, Bangalore, India for providing necessary funds to undertake this project. Financial support of Shiraz university, Iran to the second author is appreciated

REFERENCES
Alagawadi, A.R. and A.C. Gaur, 1988. Associative effect of Rhizobium and phosphate solubilizing bacteria on the yield and nutrient uptake of chickpea. Plant Soil, 105: 241-246.

Anderson, A.J. and D. Guera, 1985. Response of bean to root colonization with Pseudomonas putida in a hydroponic system. Phytopathology, 75: 992-995.

Andrade, G., F.A.A.M. De Leij and J.M. Lynch, 1998. Plant mediated interactions between Pseudomonas fluorescens, Rhizobium leguminosarum and arbuscular mycorrhizae on pea. Lett. Applied Microbiol., 26: 311-316.
CrossRef  |  Direct Link  |  

Arshad, M. and W.T. Frankenberger Jr., 1993. Microbial Production of Plant Growth Regulators. In: Soil Microbial Ecology: Application in Agricultural and Environmental Management, Metting, Jr. F.B. (Ed.). Marcel Dekker Inc., New York, USA., ISBN-13: 9780824787370, pp: 307-347.

Cakmakci, R., F. Donmez, A. Aydin and F. Sahin, 2006. Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol. Biochem., 38: 1482-1487.
CrossRef  |  Direct Link  |  

Chakraborty, U., B. Chakraborty and M. Basnet, 2006. Plant growth promotion and induction of resistance in Camellia sinensis by Bacillus megaterium. J. Basic Microbiol., 46: 186-195.
Direct Link  |  

Chan, Y.K., W.L. Barraquio and R. Knowles, 1994. N2 fixing pseudomonads and related soil bacteria. FEMS Microbiol. Rev., 13: 95-118.
Direct Link  |  

Chanway, C.P., R.A. Radley, F.B. Holl and P.E. Axlerood, 1991. Effect of Bacillus Strains on Growth of Pine (Pinus contorta Dougl.), Spruce (Picea glauca Voss.) and Douglas-fir (Pseudotsuga menziesii (MIRB.) Franco). In: The Rhizosphere and Plant Growth, Keister, D.L. and P.B. Cregan (Eds.). Kluwer, Netherlands, pp: 366.

Chen, H., M. Batley, J.W. Redmond and B.G. Rolfe, 1985. Alteration of the effective nodulation properties of a fast growing broad host range Rhizobium due to change in exopolysaccharide synthesis. J. Plant Physiol., 120: 331-349.

Dashti, N., F. Zhang, R. Hynes and D.L. Smith, 1998. Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil, 200: 205-213.
CrossRef  |  Direct Link  |  

De Freitas, J.R. and J.J. Germida, 1990. Plant growth promoting rhizobacteria for winter wheat. Can. J. Mic., 36: 265-272.
Direct Link  |  

Defreitas, J.R. and J.J. Germida, 1990. A root tissue culture system to study winter wheat-rhizobacteria interactions. Applied Mic. Biot., 33: 589-595.
Direct Link  |  

Dey, R., K.K. Pal, D.M. Bhatt and S.M. Chauhan, 2004. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol. Res., 159: 371-394.
CrossRef  |  Direct Link  |  

Enebak, S.A., G. Wei and J.W. Kloepper, 1998. Effects of plant growth-promoting rhizobacteria on loblolly and slash pine seedlings. For. Sci., 44: 139-144.
Direct Link  |  

Garcia, J.A.L., A. Probanza, B. Ramos, J.J.C. Flores and F.J.G. Manero, 2004. Effects of plant growth promoting Rhizobacteria (PGPRs) on the biological nitrogen fixation, nodulation and growth of Lupinus albus L. cv. Multolupa. Eng. Life Sci., 4: 71-77.
CrossRef  |  Direct Link  |  

Gaur, A.C., 1990. Phosphate Solubilizing Microorganisms as Biofertilizer. Omega Scientific Publishers, New Delhi, India pp: 176.

Gowda, T.K.S. and I. Watanabe, 1985. Hydrogen supported N2 fixation of Pseudomonas sp. and Azospirillum lipoferum under free living conditions and in association with rice seedlings. Can. J. Mic., 31: 317-321.

Gray, E.J. and D.L. Smith, 2005. Intracellular and extracellular PGPR: Commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol. Biochem., 37: 395-412.
Direct Link  |  

Jackson, M.L., 1973. Soil Chemical Analysis. 1st Edn., Prentice Hall Ltd., New Delhi, India, Pages: 498.

James, E.K. and F.L. Olivares, 1997. Infection of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci., 17: 77-119.
Direct Link  |  

Joshi, P.K., J.H. Kulkarni and D.M. Bhatt, 1990. Interaction Between Strains of Bradyrhizobium and Groundnut (Arachis hypogaea L.) Cultivars. Trop. Agric., 65: 115-118.
Direct Link  |  

Kapulnik, Y., Y. Okon and Y. Henis, 1985. Changes in root morphology of wheat caused by Azospirillum brasilense. Can. J. Mic., 31: 881-887.

Kloepper, J.W., 1993. Plant Growth Promoting Rhizobacteria as Biological Control Agents. In: Soil Microbial Ecology-Applications in Agricultural and Environmental Management, Metting, Jr. F. (Ed.). Marcel Dekker, New York, pp: 255-274.

Kloepper, J.W., N.M. Schroth and T.D. Miller, 1980. Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology, 70: 1078-1082.
CrossRef  |  Direct Link  |  

Kloepper, J.W., R. Rodriguez-Kabana, J.W. Zehnder, J. Murphy, E. Sikora and C. Fernandes, 1999. Plant root-bacterial interactions in biological control of soil borne diseases and potential extension to systemic and foliar diseases. Australas. Plant Pathol., 28: 21-26.
Direct Link  |  

Leigh, J.A., E.R. Singer and G.C. Walker, 1988. Exopolysaacharide deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Nat. Acad. Sci. USA., 82: 6231-6235.

Lifshitz, R., J.W. Kloepper, M. Kozlowshi, C. Simonson, J. Carlson, M. Tipping and I. Zalesha, 1987. Growth promotion of Canola (rapeseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can. J. Mic., 33: 390-395.
Direct Link  |  

Lucy, M., E. Reed and B.R. Glick, 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek, 86: 1-25.
Direct Link  |  

Mantelin, S. and B. Touraine, 2004. Plant growth-promoting bacteria and nitrate availability: Impacts on root development and nitrate uptake. J. Exper. Bot., 55: 27-34.
CrossRef  |  Direct Link  |  

Neito, K.F. and W.T. Jr. Frankenberger, 1989. Biosynthesis of cytokinins by Azotobacter chroococcum. Soil Biol. Biochem., 21: 967-972.

Nishijima, F., W.R. Evans and S.J. Vesper, 1988. Enhanced nodulation of soybean by Bradyrhizobium in the presence of Pseudomonas fluorescens. Plant Soil, 111: 149-150.

Parmar, N. and K.R. Dadarwal, 1999. Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J. Applied Microbiol., 86: 36-44.
Direct Link  |  

Petersen, D.J., M. Srinivasan and C.P. Chanway, 1996. Bacillus polymyxa stimulates increased Rhizobium etli populations and nodulation when co-resident in the rhizosphere of Phaseolus vulgaris. FEMS Microbiol. Lett., 142: 271-276.
Direct Link  |  

Pieterse, C.M.J., S.C.M. Van-Wees, J. Ton, J.A. Van-Pelt and L.C. Van-Loon, 2002. Signalling in rhizobacteria induced systemic resistance in Arabidopsis thaliana. Plant Biol., 4: 535-544.
Direct Link  |  

Polonenko, D.R., F.M. Scher, J.W. Kloepper, C.A. Singleton, M. Laliberte and I. Zalerka, 1987. Effect of root colonizing bacteria on nodulation of soybean roots by Bradyrhizobium japonicum. Can. J. Microbiol., 33: 498-503.

Preston, G.M., 2004. Plant perceptions of plant growth-promoting Pseudomonas. phil trans. R. Soc. Land. B., 359: 907-918.
CrossRef  |  

SAS, 1999. SAS/STAT User's Guide. Version 8, SAS Institute Inc., Cary, North Carolina.

Sakthivel, N., E. Sivamani, N. Unnamalai and S.S. Gnanamanickam, 1986. Plant growth promoting rhizobacteria in enhancing plant growth and suppressing plant pathogens. Curr. Sci., 55: 22-25.

Shaharoona, B., M. Arshad, Z.A. Zahir and A. Khalid, 2006. Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol. Biochem., 38: 2971-2975.
CrossRef  |  Direct Link  |  

Vessey, J.K., 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 255: 571-586.
CrossRef  |  Direct Link  |  

Wang, C., E. Knill, B.R. Glick and G. Defago, 2000. Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol., 46: 898-907.
PubMed  |  Direct Link  |  

Weller, D.M., J.M. Raaijmakers, B.B.M. Gardener and L.S. Thomashow, 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol., 40: 309-348.
CrossRef  |  PubMed  |  Direct Link  |  

©  2019 Science Alert. All Rights Reserved
Fulltext PDF References Abstract