The role of plant growth promoting Rhizobacteria (PGPR) in sustainable agriculture.
Plants are always subjected to biotic and abiotic factors in their environment which influence their growth and development. This is important from economical point of view as these factors affect the root development and production rate greatly. [25,41,42,43,44,45,46,47,48] A large number of different microorganisms, mostly bacteria, are commonly found in soil. Soil bacteria interact specifically with plant roots in the rhizosphere, where bacterial density is generally higher. The bacteria that provide benefits to the plant either form symbiotic relationships with the plant or are free-living in the soil, but found near or even within the roots . Beneficial free-living soil bacteria are usually referred to as plant-growth-promoting rhizobacteria or PGPR, [18,40,41].  The Rhizosphere is the particular zone surrounding the roots of plants, in which living creatures around it are affected quantitatively and qualitatively by root vital activities like breath and root secretion.  This soil restriction is rich in nutrition elements; because of plant systematic root activities Rhizosphere is a mixture of solid particles and active community of bacteria.  The term rhizosphere will be used to refer to both zones. In the rhizosphere, very important and intensive interactions are taking place between the plant, soil, microorganisms and soil microfauna. In fact, biochemical interactions and exchanges of signal molecules between plants and soil microorganisms have been described and reviewed.  These interactions can significantly influence plant growth and crop yields. In the rhizosphere, bacteria are the most abundant microorganisms. Rhizobacteria are rhizosphere competent bacteria that aggressively colonize plant roots; they are able to multiply and colonize all the ecological niches found on the roots at all stages of plant growth, in the presence of a competing microflora.   The presence of rhizobacteria in the rhizosphere can have a neutral, detrimental or beneficial effect on plant growth. The presence of neutral rhizobacteria in the rhizosphere probably has no effect on plant growth.  Microorganism activity in Rhizosphere depends on ecological and soil factors, plant species, plant age, and plant growth phase and soil tissue. Bacteria have the most population density between the Rhizosphere microorganisms because of high growth speed and the ability to use the various carbon and nitrogen sources. Rhizobacteria is divided into 2 groups; according to the kind of the influence over the plant's growth and development.  The first group has negative influence over the plant's growth and development; Deleterious Rhizobacteria (DRB),  The second one increases the plant's growth and development; Plant Growth Promoting Rhizobacteria (PGPR),  was named.Mainly, the Deleterious Rhizobacteria (DRB) inter their harmful detriment (damage) by producing deleterious metabolites which absorb by root, without directly interfere the plant tissue,  These metabolites include: Hydrogen cyanide(HCN),plant hormones like indole-3 Acetic acid  and unknown phytotoxins. Various soil microorganisms like: bacteria , fungus and alga, can secrete Auxin which have destructive influence over the growth and plant's settlement. Loper & Schroth, 1986 published the report about 2 strains of Enterobacteriaceae family, which decrease the root length in the inoculation time with beet plant(Beta vulgaris L.) by secreting too much IAA hormone(Indole-3- Acetic acid). Different species of DBR have been reported like: Desulfovibrio, Erwinia, Agrobacterium, Pseudomonas, Enterobacter and Chromobacter [9,24].
Plant Growth Promoting Rhizobacteria (PGPR):
About 2 to 5% of rhizobacteria, when reintroduced by plant inoculation in a soil containing competitive microflora, exert a beneficial effect on plant growth and are termed plant growth promoting rhizobacteria (PGPR) . PGPR are free-living bacteria  and some of them invade the tissues of living plants and cause unapparent and asymptomatic infections .
Plant Growth Promoting Rhizobacteria (PGPR) expression for the first time was propounded by Kloepper and Schroth and it was used especially for Fluorescent pseudomonads for a long time and just for kinds which indirectly and by controlling the plant pathogenic factor, improves the plant's growth. The following researchers like Kapulnik (1991) extended the PGPR domain by calculating the useful effects of Rhizobacteria over the plants growth directly. Today, this expression is frequently used for general soil bacteria which live near or on the surfaces of plants roots and improve their host plant growth by one or several certain mechanisms.  Totally the PGPR are divided into two following groups:
1- Plant growth promoting bacteria which creates symbiosis with plants. Some species like Rhizobium, Bradyrhizobium and Azospirillum are in symbiosis with Legume plants. Ektinomist Frankia is in Ektinoreyzi symbiosis and seyanobacteria is in Gunera symbiosis. These are the most important PGPR bacteria .
2- Plant growth promoting bacteria which they have the ability to promote the plant growth without creating symbiosis with plants. This kind of bacteria have good ability for Root colonization and increase the host plant growth by using different mechanisms .
Nowadays using various PGPR for improving the plant growth, decreasing the chemical fertilizer pollution and pesticides are became widely practice in many parts of the world like Brazil, India, America, Argentina, Uruguay which are sold as Growth Promoting inoculationtion liquid or biologic Pesticides.  PGPR bacteria usage in China with the Yield Increasing Bacteria has been initiated in 1979. Today these bacteria has been used in 30 provinces(states) for 55 products and their minimum economical benefits are 59/4 million dollar yearly. Because of high potential of Rhizosphere growth promoting bacteria in producing plant hormones and decreasing the damage of the plant pathogen factor, in recent years they are used as root promoting hormone and Biocontrol factors. In many parts of the world, they are used as stimulators and Biocontrol to improve the plant growth and decrease the pollution of the chemical fertilizer pollution and pesticides.
PGPR may induce plant growth promotion by direct or indirect modes of action.  Direct mechanisms include the production of stimulatory bacterial volatiles and phytohormones, lowering of the ethylene level in plant, improvement of the plant nutrient status (liberation of phosphates and micronutrients from insoluble sources; non-symbiotic nitrogen fixation) and stimulation of disease-resistance mechanisms (induced systemic resistance). Indirect effects originate for example when PGPR act like biocontrol agents reducing diseases, when they stimulate other beneficial symbioses, or when they protect the plant by degrading xenobiotics in inhibitory contaminated soils . Based on their activities classified PGPR as biofertilizers (increasing the availability of nutrients to plant), phytostimulators (plant growthpromoting, usually by the production of phytohormones), rhizoremediators (degrading organic pollutants) and biopesticides (controlling diseases, mainly by the production of antibiotics and antifungal metabolites). 
Recognized Species as Plant Growth Promoting Bacteria:
 proposed the division of PGPR into two classes: biocontrol-PGPB (plant-growth-promoting-bacteria) and PGPB. This classification may include beneficial bacteria that are not rhizosphere bacteria but it does not seem to have been widely accepted.  When studying beneficial rhizobacteria, the original definition of PGPR is generally used: it refers to the subset of soil and rhizosphere bacteria colonizing roots in a competitive environment, e.g. in non-pasteurized or non-autoclaved field soils.  Furthermore, in most studied cases, a single PGPR will often reveal multiple modes of action including biological control .
Various kinds of Plant growth promoting bacteria are reported, some of them are as follow:
Flavobacterium, Acetobacter, Pseudomonas, Azos pirillum, Azotobacter, Arthrobacter, Micrococus, Chro mobacterium, Agrobacterium, Bacillus, Burkholderia, Erwinia, Hypomycrobium, Xanthomonas, Klebsiella [11,28,22].
Azospirillum known for many years as PGPR was isolated from the rhizosphere of many grasses and cereals all over the world, in tropical as well as in temperate climates.  This bacterium was originally selected for its ability to fix atmospheric nitrogen (N2), and since the mid-1970s, it has consistently proven to be a very promising PGPR, and recently the physiological, molecular, agricultural and environmental advances made with this bacterium were thoroughly reviewed by.  Presently PGPR for which evidence exists that their plant stimulation effect is related to their ability to fix N2 include the endophytes Azoarcus sp., Burkholderia sp., Gluconacetobacterdiazotrophicus and Herbaspirillum sp. and, the rhizospheric bacteria Azotobacter sp. and Paenibacillus (Bacillus) polymyxa .
Flavobacterium, Pseudomonas, Arthrobacter are species of bacteria that are around the soil of the roots and Rhizosphere  In a research Kleeberger and his colleague in 1983 observed that wheat Rhizosphere and Pseudomonas have the most population accumulation .
 showed that the majority (95%) of Gram-positive bacteria in soils under different types of management regimes (permanent grassland, grassland turned into arable land, and arable land), were putative Bacillus species; B. mycoides, B. pumilus, B.megaterium, B. thuringiensis, and B. firmus, as well as related taxa such as Paenibacillus, were frequently identified by sequencing the DNA bands obtained on DGGE gels. Other Gram-positive bacteria including Arthrobacter spp. and Frankia spp. were a minority (less than 6% of the clones obtained).  The ubiquity and the importance of B. benzoevorans in soils throughout the world were proved by using molecular methodology developed to identify non-culturable bacteria.  Bacillus spp. are able to form endospores that allow them to survive for extended periods under adverse environmental conditions. Some members of the group are diazotrophs and B. subtilis was isolated from the rhizosphere of a range of plant species at concentration as high as 107 pergram of rhizosphere soil.[39,9].
Early observations on the beneficial effect of seeds or seed pieces bacterization were first made with Pseudomonas spp. isolates, on root crops. By treating potato (Solanum tuberosum L.) seed pieces with suspensions of strains of Pseudomonas fluorescens and P. putida,  obtained statistically significant increases in yield ranging from 14 to 33% in five of nine field plots established in California and Idaho .
Many Fluorescent Pseudomonads, especially P. putida and P. fluorescence promote the plant growth and have the ability to increase the Crop yield  Producing many second metabolite by pseudomonas, emphasizes over using the agricultural, industrial and healthy aims .
Among the Gram-negative bacteria, Pseudomonaceae family is a large and an important group .
They were found in the natural environment, water, soil and even with plant and animals in the form of normal microflora or as a pathogenic factor. In morphology, these microorganisms are gram-negative, without spore, curved or straight rod, and movable with one or more polar flagellum (monotrichous: having a single polar flagellum.  Four species of Pseudomonas, Xanthomonas, Zoog loes, Frateuria are in this family. All of these species are Chemoorganotroph with aerobic metabolism, non-fermentative and non-photosynthesis. They grow in the basic environment because of their simple nutritious need. Because of aerobic activity they have major role in carbon-cycle. Differences among these four Pseudomonaceae are proved in the Pseudomonas fluorescens route.  In the P.fluorescens ATCC 29574 the IAA synthesis is initiated from the (TSO-tryptophan side chain oxidas) route. In the TSO side chain oxidization route, the indole-3-acetaldehyde has intermediate role , which forms IAA from the oxidization of the acetaldehyde dehydrogenize enzyme. TSO enzyme just has activity in the growth bacteria static phase against the tryptophan Trans Aminaz which are active in the Logarithmic and static phases  .TSO route has more activity to produce IAA, in acidic PH . IAA production in PH, is decreased in the IPYA route .
Rhizobia and bradyrhizobia are well known as the microbial symbiotic partners of legumes, forming N2-fixing nodules. However these bacteria also share many characteristics with other PGPR. In fact rhizobia can produce phytohormones, siderophores, HCN; they can solubilize sparingly soluble organic and inorganic phosphates, and they can colonize the roots of many non-legume plants.  Under greenhouse condition, radish dry matter yield was increased by inoculation with strains of Bradyrhizobium japonicum, Rhizobium leguminosarum bv. phaseoli, R. leguminosarum bv. trifolii, R. leguminosarum bv. viciae and Sinorhizobium meliloti. The highest stimulatory effect (60% increases as compared to the uninoculated control) was observed with strain Soy213 of B. japonicum .
[1.] Alizadeh, O., K. Ordookhani, 2011. Use of N2-fixing Bacteria Azotobacter, Azosprilium in Optimizing of Using Nitrogen in Sustainable Wheat Cropping, Advances in Environmental Biology, 5(7): 1572-1574.
[2.] Antoun, H. and J.W. Kloepper, 2001. Plant growth-promoting rhizobacteria (PGPR), in :Encyclopedia of Genetics, Brenner, S. and Miller, J.H., eds., Academic Press, N.Y., pp:1477-1480.
[3.] Antoun, H., C.J. Beauchamp, N. Goussard, R. Chabot and R. Lalande, 1998. Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on nonlegumes:effect on radishes (Raphanus sativus L.), Plant Soil, 204: 57-67.
[4.] Bashan, Y., G. Holguin and L.E. de-Bashan, 2004. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003), Can. J. Microbiol., 50: 521-577.
[5.] Burr, T.J., Schroth, M.N. and T. Suslow, 1978. Increased potato yields by treatment ofseedpieces with specific strains of Pseudomonas fluorescens and P. putida, Phytopathology, 68: 1377-1383.
[6.] Davison, J., 1988. Plant beneficial bacteria. Biotechnol., 6: 282-286.
[7.] Frommel, M.I., J. Nowak, G. Lazarovits, 1991. Growth enhancement and development modifications of in vitro grown potato (Solanum tuberosum ssp. tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiol., 96: 928-936.
[8.] Garbeva, P., J.A. Van Veen and J.D. Van Elsas, 2003. Predominant Bacillus spp. In agricultural soil under different management regimes detected via PCR-DGGE, Microb Ecol. 45: 302316.
[9.] Gupta, A., A.K. Saxena, M. Gopal and V.B.R. Tilak, 2003. Effects, of co-inoculation of plant growth promoting rhizobacteria and Bradyrhizobium sp (Vigna) on growth and yield of green gram [Vigna radiata (L.) Wilczek], Trop. Agr., 80: 28-35.
[10.] Guttierrez-Zamora, M.L. and E. Martinez-Romero, 2001. Natural endophytic association between Rhizobium etli and maize (Zea mays L.), J. biotechnol., 91: 177-126.
[11.] Gray, E.J. and D.l. Smith, 2004. Inttracellular and extracellular PGPR.Soil iol.Biochem., 5: 118.
[12.] Glick, B.R., C.L. Patten, G. Holguin and D.M. Penrose, 1999. Biochemical and genetic mechanisms used by plant growth promoting bacterial Cllege Press London United Kingdom, pp: 267.
[13.] Glick, B.R., 2005. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase, FEMS Microbiology Letters, 251: 1-7.
. Jacobsen, C.S., 1997. Plant protection and rhizosphere colonization of barley by seed inoculated herbicide degrading Burkholderia (Pseudomonas) cepacia DBO1(pRO101) in 2,4 D contaminated soil, Plant Soil, 189: 139-144.
[15.] Jacobson, C.B., Pasternak, J.J. and B.R. Glick, 1994. Partial purification and characterization of ACC deaminase from the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2, Can. J. Microbiol., 40: 1019-1025.
[16.] Kapulink, Y., S. Sarig, I. Nur, Y. Okon, J. Kigel and U. Henit, 1991. Yield increases isomer cereal crops of Israel in fields inoculated with Azosprillum. Experientia Agricola., 17: 179187.
[17.] Kloepper, J.W. and M.N. Schroth, 1978. Plant growth- promoting rhizobacteria on radishes. In Proceedings of the 4th International Conference on Plant Pathogenic Bacteria., Pp: 879-882.
[18.] Kloepper, J.W., R. Lifshit and R.M. Zablotwicz, 1989. Free-living bacterial inoculation for enhancing crop productivity. Trends Biotechnol., 7: 39-43.
[19.] Kloepper, J.W., 2003. A review of mechanisms for plant growth promotion by PGPR, in: Abstracts and short papers. 6th International PGPR workshop, 5-10 october 2003. M.S., Reddy, M., Anandaraj, S.J., Eapen, Y.R., Sarma and J.W., Kloepper, eds., Indian Institute of Spices Research, Calicut, India, pp: 81-92.
[20.] Kloepper, J.W., B. Schippers and P.A.H.M. Bakker, 1992. Proposed elimination of the term endorhizosphere, Phytopathol., 82: 726-727.
[21.] Lazarovits, G. and J. Nowak, 1997. Rhizobacteria for improvement of plant growth and establishment, HortScience, 32: 188-192.
[22.] Misko, A.L. and J.J. Germida, 2002. Taxonomy and functional diversity of pseudomonads isolated from the root of field grown canola. FEMS Microbial. Ecol., 42: 399-407.
[23.] Ordookhani, K., 2011. Investigation of PGPR on Antioxidant Activity of Essential Oil and Microelement Contents of Sweet Basil. Advances in Environmental Biology, 5(6): 11141119.
[24.] Ordookhani, K. and M. Zare, 2011. Effect of Pseudomonas, Azotobacter and Arbuscular Mycorrhiza Fungi on Lycopene, Antioxidant Activity and Total Soluble Solid in Tomato (Lycopersicon Esculentum F1 Hybrid, Delba. Advances in Environmental Biology, 5(6): 12901294.
[25.] Parsaeimehr, A.O., Alizadeh, B. jafari, 2009. Applying azespiriliom bacteria and interaction of it with stereptomyces spp due biological control on wheat(triticum asstivum) sustainable culture. american-eurasian journal of sustainable agriculture, 3(3): 622-625.
[26.] Schippers, B., A.W. Bakker, P.A.H.M. Bakker, and R. Vanpeer, 1990. Beneficial and deleterious effects of HCN- production Pseudomonads on rhizosphere interaction. Plant Soil., pp: 129.
[27.] Somers, E., J. Vanderleyden and M. Srinivasan, 2004. Rhizosphere bacterial signalling: alove parade beneath our feet, Crit. Rev. Microbiol., 30: 205-240.
[28.] Steenhoudt, O., and J. Vanderleyden, 2000, Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses :genetic, biochemical and ecological aspects, FEMS Microb. Rev., 24: 487-506.
[29.] Sturz, A.V. and J. Nowak, 2000. Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops, Appl. Soil Ecol., 15 :183-190.
[30.] Tzeneva, V.A., Y. Li, A.D.M. A.D.M. Fleske, W.M. de Vos, A.D.L. Akkermans, E.E. Vaughan and H. Smidt, 2004. Development and application of a selective PCR-denaturing gradient gel electrophoresis approach to detect a recently cultivated Bacillus group predominant in soil, Appl. Environ. Microbiol., 70: 58015809, 75-83.
. Van, Peer R., B. Schippers, 1989. Plant growth responses to bacterization with selected Pseudomonas spp. strains and rhizosphere microbial development in hydroponic cultures. Can J Microbiol., 35: 456-463.
[32.] Vessey, J.K., 2003. Plant growth promoting rhizobacteria as biofertilizers, Plant Soil., 255: 571-586.
[33.] Vivas, A., B. Biro, E. Campos, J.M. Barea and R. Azcn, 2003a. Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mossae) and Brevibacillus sp. Isolated from cadmium polluted soil under increasing cadmium levels. Environ. Pollut., 126: 179-189.
[34.] Vivas, A., R. Azcn, B. Biro, J.M. Barea and J.M. Ruiz-Lozano, 2003b. Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscularmycorrhizae on the growth of Trifolium pratense L. under lead toxicity, Can J Microbiol., 49: 577-588.
[35.] Von Bodman, S.B., W.D. Bauer and D.L. Coplin, 2003. Quorum sensing in plantpathogenic bacteria, Annu. Rev. Phytopathol., 41: 455-481.
[36.] Vlassak, K., L.V. Holm, L. Duchateau, J. Vanderleyden and R.D. Mot, 1992. Isolation and characterization of Fluorescent pseudomonads associated with the roots of rice and banana grown in srilanka. Pland Soil., 145: 51-63.
[37.] Werner, D., 2001. Organic signals between plants and microorganisms. in: The Rhizosphere. Biochemistry and Organic Substances at the Soil-Plant Interface. Pinton, R., Varanini, Z. and Nannipieri, P., eds. Marcel Dekker, Inc. N.Y., pp: 197-222.
[38.] Werner, D., 2004. Signalling in the rhizobia-legumes symbiosis, in: Plant surface microbiology. Varma, A., Abbott, L., Werner, D., Hampp, R., eds Springer, N.Y., pp: 99-119.
[39.] Winding, A., S.J. Binnerup and H. Pritchard, 2004. Non-target effects of bacterial control agents suppressing root pathogenic fungi, FEMS Microbiol. Ecol., 47: 129-141.
[40.] Wipat, A. and C.R. Harwood, 1999. The Bacillus subtilis genome sequence: the molecular blueprint of a soil bacterium, FEMS Microb. Ecol., 28: 1-9.
[41.] Ordookhani, K., 2011. Investigation of PGPR on Antioxidant Activity of Essential Oil and Microelement Contents of Sweet Basil. Advances in Environmental Biology, 5(6): 11141119.
[42.] Mahmood, M., Z. Abdul Rahman, H. Mohd. Saud, Zi Shamsuddin and S. Subramaniam, 2009. Responses of Banana Plantlets to Rhizobacteria Inoculation under Salt Stress Condition, American-Eurasian Journal of Sustainable Agriculture, 3(3): 290-305.
[43.] Sadeghi, H., 2009. Effects of Different Levels of Sodium Chloride on Yield and Chemical Composition in Two Barley Cultivars, American-Eurasian Journal of Sustainable Agriculture, 3(3): 314-320.
[44.] Rahimi, A. and A. Biglarifard, 2011. Impacts of NaCl Stress on Proline, Soluble Sugars, Photosynthetic Pigments and Chlorophyll Florescence of Strawberry. Advances in Environmental Biology, 5(4): 617-623.
[45.] Mahmoodabad, R.Z., Somarin S.J., M. Khayatnezhad and R. Gholamin. The study of effect salinity stress on germination and seedling growth in five different genotypes of wheat. Advances in Environmental Biology, 5(1): 177179.
[46.] Homayoun, H., 2011. Effect of NaCl Salinity on Wheat (Triticum aestivum L.) Cultivars at Germination Stage. Advances in Environmental Biology, 5(7): 1716-1720.
[47.] Suleiman, M.N., S.A. Emua and A. Taiga, 2008. Effect of Aqueous Leaf Extracts on a Spot Fungus (Fusarium Sp) Isolated from Compea, American-Eurasian Journal of Sustainable Agriculture., 2(3): 261-263.
[48.] Taiga, A. and E. Friday, 2009. Vriations in Phytochemical Properties of Selected Fungicidal Aqueous Extracts of Some Plant Leaves in Kogi State, Nigeria, American-Eurasian Journal of Sustainable Agriculture, 3(3): 407-409.
[49.] Asgharipour, M.R., M. Armin, 2010. Inhibitory effects of Sorghum halepens root and leaf extracts on germination and early seedling growth of widely used medicinal plants. Advances in Environmental Biology, 4(2): 316-324.
(1) Barmak Jafari Haghighi, (2) Omid Alizadeh and (2) Alireza Hedayati Firoozabadi
(1) Department of Agriculture, Arsenjan Branch, Islamic Azad University, Arsenjan, Iran.
(2) Department of Agriculture, Firooz Abad Branch, Islamic Azad University, Firooz Abad, Iran.
Barmak Jafari Haghighi, Omid Alizadeh and Alireza Hedayati Firoozabadi: The Role of Plant Growth Promoting Rhizobacteria (PGPR) in Sustainable Agriculture.
Barmak Jafari Haghighi, Department of Agriculture, Arsenjan Branch, Islamic Azad University Arsenjan, Iran. Tel: 9173107299
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||Original Article|
|Author:||Haghighi, Barmak Jafari; Alizadeh, Omid; Firoozabadi, Alireza Hedayati|
|Publication:||Advances in Environmental Biology|
|Date:||Sep 1, 2011|
|Previous Article:||Groundwater suitability for irrigation in the Damghan region, Semnan province, Iran.|
|Next Article:||Effect of plant density and nitrogen rate on yield and yield components of wheat in wild oat-infested condition.|