Plant Growth Promoting Rhizobacteria A review

A. Benaissa


Abstract : Plant Growth Promoting Rhizobacteria (PGPR) are the rhizospheric bacteria that can affect positively plant growth by several mechanisms like phosphate solubilization, siderophore production, biological nitrogen fixation, production of 1-Aminocyclopropane-1-carboxylate deaminase (ACC), quorum sensing (QS) signal interference and inhibition of biofilm formation, phytohormone production, exhibiting antimicrobial activity, induction of systemic resistance (ISR), promoting beneficial plant-microbe symbioses, and many others mechanismms. It is the biological way to replace the use of chemical fertilizers, pesticides in agriculture practices. The PGPR strains present a high taxonomic and metabolic diversity. This review synthesizes the different aspects of PGPR studies, from their applications to the stress tolerance, via the different modes of action.

Full Text:



Sorensen, J. The rhizosphere as a habitat for soil microorganisms. In Book Modern soil microbiology, Elsas, J.D.; Van Trevors J.T.; Dekker, M: Wellington, New York, 1997; Volume 56, pp. 21-45.

Kennedy, A.C. The rhizosphere and spermosphere. In : Principles and applications of soil microbiology, Sylvia, D.M.; Fuhrmann, J.J.; Hartel, P.G.; Zuberer, D.A.; Prentice Hall, Upper Saddle River, New Jersy, 1999; pp. 389-407

Boehm, M.; Madden, V.; Hoitink, H.A.J. Effect of organic matter decomposition level on bacterial species diversity and composition in relation to Pythium damping off severity. Applied and Environmental Microbiology 59 (1993) 4171-4179.

Kloepper, J.W.; Beauchamp, C. J. A review of issues related to measuring colonization of plant roots by bacteria. Canadian. Journal of Microbiology 38 (1992) 1219-1232.

Gobat, J. M. ; Aragno, M.; Matthey, W. Le sol vivant : bases de pédologie, biologie des sols. PPUR Presses polytechniques. 2010 (14).

Bais, H.P.; Weir, T.L.; Perry, L.G.; Gilroy, S.; Vivanco, J.M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual. Review of Plant Biology 57 (2006) 233–266.

Voisard, C.; Keel, C.; Haas, D.; Defago, G. Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. The EMBO Journal 8 (1989) 351-358.

Van Peer, R.; Niemann, G.J.; Schippers, B. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS 417 r. Phytopathology 81 (7) (1991) 728-734.

Kloepper J.W.; Ryu C.M.; Zhang S. Induced systemic resistance and promotion of plant growth by Bacillus species. Phytopathology 94 (2004) 1259-1266.

Orhan, E.; Esitken A.; Ercisli S.; Turan, M.; Sahin, F. Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Scientia Horticulturae 111 (2006) (1) 38-43.

Glick, B.R. The enhancement of plant growth by free-living bacteria. Canadian journal of microbiology 41 (2) 109-117.

Fernando, W. D.; Nakkeeran, S.; Zhang, Y. Biosynthesis of antibiotics by PGPR and its relation in biocontrol of plant diseases. In PGPR : Biocontrol and Biofertilization, Springer Netherlands (2005) 67-109.

Kloepper, J.W. Plant growth-promoting rhizobacteria as biological control agents. In Soil Microbial Ecology: Applications in Agricultural and Environmental Management. Marcel Dekker Inc., New York, 1992; pp. 255-274.

Kloepper, J. W.; Lifshitz, R.; Zablotowicz, R. M. Free-living bacterial inocula for enhancing crop productivity. Trends in biotechnology 7 (2) (1989) 39-44

Zahir, Z. A.; Arshad, M.; Frankenberger, W. T. Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Advances in Agronomy 81 (2004) 98-169.

Gamalero, E.; Berta, G.; Glick, B.R. The use of microorganisms to facilitate the growth of plants in saline soils. In Microbial strategies for crop improvement, Springer, Berlin, Heidelberg. (2009) 1-22

Kloepper, J. W.; Schroth, M. N. Plant growth-promoting rhizobacteria on radishes. In Proceedings of the 4th international conference on plant pathogenic bacteria 2 (1978) 879-882.

Hallmann, J.; Quadt-Hallmann, A.; Mahaffee, W.F.; Kloepper, J.W. Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology, 43 (10) (1997) 895-914.

Beauchamp, C.J. Mode d’action des rhizobactéries favorisant la croissance des plantes et potentiel de leur utilisation comme agent de lutte biologique. Phytoprotection 74 (1) (1993)19-27.

Vessey, J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant and soil 255 (2) (2003) 571-586.

Tamilarasi, S.; Nanthakumar, K.; Karthikeyan, K.; Lakshmanaperumalsamy, P. Diversity of root associated microorganisms of selected medicinal plants and influence of rhizomicroorganisms on the antimicrobial property of Coriandrum sativum. Journal of environmental biology 29 (1) (2006) 127.

Saharan, B.S.; Nehra, V. Plant growth promoting rhizobacteria: a critical review. Life Sciences and Medicine Research 21 (1) (2001) 30.

Adesemoye, A.O.; Torbert, H.A.; Kloepper, J.W. Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microbial Ecology 58 (4) (2009) 921-929.

Amir, H.G.; Shamsuddin, Z.H.; Halimi, M. S., Marziah, M., Ramlan, M. F. Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Communications in soil science and plant analysis 36 (15-16) (2005) 2059-2066.

Bashan, Y.; Holguin, G.; De-Bashan, L.E. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Canadian journal of microbiology 50 (8) (2004) 521-577.

Saleem, M.; Arshad, M.; Hussain, S.; Bhatti, A.S. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. Journal of industr

ial microbiology & biotechnology 34 (10) (2007) 635-648.

Gururani, M.A.; Upadhyaya, C.P.; Baskar, V.; Venkatesh, J.; Nookaraju, A.; Park, S.W. Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. Journal of Plant Growth Regulation 32 (2) (2013) 245-258.

Jaleel, C. A.; Manivannan, P.; Sankar, B.; Kishorekumar, A.; Gopi, R.; Somasundaram, R.; Panneerselvam, R. Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids and Surfaces B : Biointerfaces 60 (1) (2007) 7-11.

Hoitink, H.A. J.; Boehm, M. J. Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annual review of phytopathology 37 (1) (1999) 427-446.

Rovira, A.D.; Elliott, L.F.; Cook, R.J. The impact of cropping systems on rhizosphere organisms affecting plant health. The impact of cropping systems on rhizosphere organisms affecting plant health (1990) 389-436.

Kloepper, J.W. Plant growth-promoting rhizobacteria (other systems). Azospirillum/plant associations (1994) 137-166.

Hugenholtz, P. Exploring prokaryotic diversity in the genomic era. Genome biology 3 (2) (2002) 3-1.

Bashan, Y.; G. Holguin., L.E. De-BashanAzospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Canadian journal of microbiology 50 (2004) 521-577.

McNeill, A.; Unkovich, M. The nitrogen cycle in terrestrial ecosystems. In Nutrient cycling in terrestrial ecosystems Springer, Berlin, Heidelberg. (2007) 37-64.

Ramette, A.; Moënne-Loccoz, Y.; Défago, G. Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot. FEMS microbiology ecology 44 (1) (2003) 35-43.

Mackie, A.E.; Wheatley, R.E. Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biology and Biochemistry 31 (3) (1999) 375-385.

Castric, P.A. Glycine metabolism by Pseudomonas aeruginosa: hydrogen cyanide biosynthesis. Journal of Bacteriology 130 (2) (1977) 826-831.

Ashrafuzzaman, M.; Hossen, F.A.; Ismail, M.R.; Hoque, A.; Islam, M.Z.; Shahidullah, S.M.; Meon, S. Efficiency of plant growth-promoting rhizobacteria (PGPR) for the enhancement of rice growth. African Journal of Biotechnology 8 (7) (2009).

Patten, C. L.; Glick, B. R. Bacterial biosynthesis of indole-3-acetic acid. Canadian journal of microbiology 42 (3) (1996) 207-220.

Loper, J. E.; Schroth, M. N. Influence of bacterial sources of indole-3-acetic acid on root elongation of sugar beet. Phytopathology 76 (4) (1986) 386-389.

Richardson, A.E.; Barea, J.M.; McNeill, A.M.; Prigent-Combaret, C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and soil 321 (1-2) (2009) 305-339.

Glick, B. R.; Penrose, D. M.; Li, J. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. Journal of theoretical biology 190 (1) (1998) 63-68.

Lemanceau, P.; Bauer, P.; Kraemer, S.; Briat, J.F. Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes. Plant and Soil 321 (1-2) (2009) 513-535.

Robin, A.; Vansuyt, G.; Hinsinger, P.; Meyer, J. M.; Briat, J.F.; Lemanceau, P. Iron dynamics in the rhizosphere: consequences for plant health and nutrition. Advances in agronomy 99 (2008) 183-225

Igual, J.; Valverde, A.; Cervantes, E.; Velázquez, E. Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21 (6-7) (2001) 561-568.

Rodrı́guez, H.; Fraga, R. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology advances, 17 (4-5) (1999) 319-339.

Jakobsen, I.; Leggett, M. E.; Richardson, A. E. Rhizosphere microorganisms and plant phosphorus uptake. Phosphorus : Agriculture and the Environment (phosphorusagric) (2009) 437-494.

Mohammadi, K. Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Resources and Environment 2 (1) (2012) 80-85.

Oehl, F.; Frossard, E.; Fliessbach, A.; Dubois, D.; Oberson, A. Basal organic phosphorus mineralization in soils under different farming systems. Soil Biology and Biochemistry 36 (4) (2004) 667-675.

Cocking, E.C. Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant and soil 252 (1) (2003) 169-175.

Kumar, A.; Prakash, A.; Johri, B.N. Bacillus as PGPR in crop ecosystem. In Bacteria in agrobiology, Maheshwari Dinesh K.; crop ecosystems, Springer, Berlin, Heidelberg, 2011; pp.37-59

Gupta, A.; Gopal, M.; Tilak, K.V. Mechanism of plant growth promotion by rhizobacteria. Indian Journal of Experimental Biology 38 (2000) 856-862.

Rakotoarimanga, N.; Zananirina, J.; Ramamonjisoa, D. ; Ramanankierana, H. Lutte biologique antifongique : actinomycètes du sol rhizosphérique antagonistes de Fusarium isolé du fruit de tomate (Solanum lycopersicum L., 1753) pourri. Afrique Science : Revue Internationale des Sciences et Technologie 10 (3) (2014).

Buchenauer, H. Biological control of soil-borne diseases by rhizobacteria/Biologische Bekämpfung von bodenbürtigen Krankheiten durch Rhizobakterien. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz/Journal of Plant Diseases and Protection (1998) 329-348.

Bolwerk, A.; Lagopodi, A. L.; Wijfjes, A. H.; Lamers, G. E., Chin-A-Woeng, T. F.; Lugtenberg, B. J.; Bloemberg, G. V. Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f. sp. radicis-lycopersici. Molecular Plant-Microbe Interactions 16 (11) (2003) 983-993.

Weller, D.M. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual review of phytopathology 26 (1) (1988) 379-407.

Alabouvette, C.; Olivain, C.; Steinberg, C. Biological control of plant diseases: the European situation. European journal of plant pathology 114 (3) (2006) 329-341.

Neilands, J.B. Siderophores: structure and function of microbial iron transport compounds. Journal of Biological Chemistry 270 (45) (1995) 26723-26726.

Lemanceau, P.; Bakker, P.A.; De Kogel, W. J., Alabouvette, C.; Schippers, B. Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Applied and Environmental Microbiology 58 (9) (1992) 2978-2982.

Nannipieri, P.; Kandeler, E.; Ruggiero, P. Enzyme activities and microbiological and biochemical processes in soil. Enzymes in the environment. Marcel Dekker, New York, (2002) 1-33

Kobayashi, D.Y.; Nour, E.H. Selection of bacterial antagonists using enrichment cultures for the control of summer patch disease in Kentucky bluegrass. Current Microbiology 32 (2) (1996) 106-110.

Ordentlich, A.; Elad, Y.; Chet, I. The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78 (1) (1988) 84-88.

Sivasakthi, S.; Usharani, G.; Saranraj, P. Biocontrol potentiality of plant growth promoting bacteria (PGPR)-Pseudomonas fluorescens and Bacillus subtilis: a review. African Journal of Agricultural Research, 9 (2014) (16) 1265-1277.

Ahmadzadeh, M.; Tehrani, A. S. Evaluation of fluorescent pseudomonads for plant growth promotion, antifungal activity against Rhizoctonia solani on common bean, and biocontrol potential. Biological Control, 48(2009) (2), 101-107.

Stutz, E.W.; Défago, G.; Kern, H. Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76 (1986) (2) 181-185.

Fatima, Z.; Saleemi, M.; Zia, M.; Sultan, T.; Aslam, M.; Rehman, R.; Chaudhary, M. F. Antifungal activity of plant growth-promoting rhizobacteria isolates against Rhizoctonia solani in wheat. African Journal of Biotechnology 8 (2009) (2)

Thomashow, L.S.; Weller, D. M. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. Journal of bacteriology 170 (1989) (8) 3499-3508.

Recep, K.; Fikrettin, S.; Erkol, D ; Cafer, E. Biological control of the potato dry rot caused by Fusarium species using PGPR strains. Biological Control 50 (2009) (2) 194-198.

Maurhofer, M.; Reimmann, C.; Schmidli-Sacherer, P.; Heeb, S.; Haas, D.; Défago, G. Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88 (7) (1998) 678-684.

Coventry, D. R.; Evans, J. Symbiotic nitrogen fixation and soil acidity. In Soil Acidity and Plant Growth (1989) 103-137.

Dakora, F. D.; Phillips, D. A. Root exudates as mediators of mineral acquisition in low-nutrient environments. In Food Security in Nutrient-Stressed Environments: Exploiting Plants’ Genetic Capabilities Springer, Dordrecht. 2002 (201-213).

Gahoonia, T.S. Influence of root-induced pH on the solubility of soil aluminium in the rhizosphere. Plant and Soil 149 (2) (1993) 289-291.

Boddey, R.M.; Urquiaga, S.; Alves, B.J.; Reis, V. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant and soil 252 (1) (2003) 139-149.

Egamberdiyeva, D.; Höflich, G. Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biology and Biochemistry 35 (7) (2003) 973-978.

Landa, B.B.; Navas‐Cortés, J.A.; Jiménez‐Díaz, R.M. Influence of temperature on plant–rhizobacteria interactions related to biocontrol potential for suppression of fusarium wilt of chickpea. Plant Pathology 53 (3) (2004) 341-352.

Zhang, F.; Dashti, N.; Hynes, R.K.; Smith, D.L. Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Annals of Botany 77 (5) (1996) 453-460.

Nautiyal, C.S.; Bhadauria, S.; Kumar, P.; Lal, H.; Mondal, R.; Verma, D. Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiology Letters 182 (2) (2000) 291-296.

Boncompagni, E.; Østerås, M.; Poggi, M.C.; le Rudulier, D. Occurrence of choline and glycine betaine uptake and metabolism in the family Rhizobiaceae and their roles in osmoprotection. Applied and environmental microbiology, 65 (5) (1999) 2072-2077.

Le Rudulier, D.; Bernard, T. Salt tolerance in Rhizobium: a possible role for betaines. FEMS Microbiology Letters 39 (1-2) (1986) 67-72.

Batzli, J.M.; Graves, W.R.; Van Berkum, P. Diversity among rhizobia effective with Robinia pseudoacacia L. Applied and Environmental Microbiology 58 (7) (1992) 2137-2143.

Graham, P.H. Short Communication Antibiotic Sensitivities of the Root Nodule Bacteria. Australian Journal of Biological Sciences 16 (2) (1963) 557-560.

Maâtallah, J.; Sanjuan, J.; Lluch, C. Phenotypic characterization of rhizobia isolated from chickpea (Cicer arietinum) growing in Moroccan soils. Agronomie 22 (3) (2002) 321-329.

Gillis, M.; Van Van, T.; Bardin, R.; Goor, M.; Hebbar, P.; Willems, A.; ... , Fernandez, M.P. Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. International Journal of Systematic and Evolutionary Microbiology 45(2) (1995) 274-289.

Giller, K. E.; Witter, E.; Mcgrath, S.P. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil biology and biochemistry 30 (10-11) (1998) 1389-1414.

Appanna, V.D.; Preston, C. M. Manganese elicits the synthesis of a novel exopolysaccharide in an arctic Rhizobium. FEBS letters 215 (1) (1987) 79-82.

Khan, M. S., Zaidi, A., Wani, P. A., Ahemad, M., & Oves, M. Functional diversity among plant growth-promoting rhizobacteria: current status. In Microbial strategies for crop improvement Springer Berlin Heidelberg. (2009) 105-132

Tien, T. M.; Gaskins, M.H.; Hubbell, D.H. Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Applied and Environmental Microbiology 37 (5) (1979) 1016-1024.

Janzen, R.A.; Rood, S.B.; Dormaar, J.F., McGill, W.B. Azospirillum brasilense produces gibberellin in pure culture on chemically-defined medium and in co-culture on straw. Soil Biology and Biochemistry 24 (10) (1992) 1061-1064

Palumbo, J.D.; Yuen, G.Y.; Jochum, C.C.; Tatum, K.; Kobayashi, D.Y. Mutagenesis of β-1, 3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95 (6) (2005) 701-707.

Walker, V. Impact de l’inoculation de micro-organismes phytobénéfiques sur le métabolisme secondaire de Zea mays L (Doctoral dissertation, Université Claude Bernard-Lyon I) (2010) 85-87.


  • There are currently no refbacks.