Rhizosphere: its structure, bacterial diversity and significance

Review paper
First Online:

Abstract

Sustainable agricultural practices are the answer to multifaceted problems that have resulted due to prolonged and indiscriminate use of chemical based agronomic tools to improve crop productions for the last many decades. The hunt for suitable ecofriendly options to replace the chemical fertilizers and pesticides has thus been aggravated. Owing to their versatile and unmatchable capacities microbial agents offer an attractive and feasible option to develop the biological tools to replace/supplement the chemicals. Exploring the microorganisms that reside in close proximity to the plant is thus a justified move in the direction to achieve this target. One of the most lucrative options is to look into the rhizosphere. Rhizosphere may be defined as the narrow zone of soil that surrounds and get influenced by the roots of the plants. It is rich in nutrients compared to the bulk soil and hence exhibit intense biological and chemical activities. A wide range of macro and microorganisms including bacteria, fungi, virus, protozoa, algae, nematodes and microarthropods co-exist in rhizosphere and show a variety of interactions between themselves as well as with the plant. Plant friendly bacteria residing in rhizosphere which exert beneficial affect on it are called as plant growth promoting rhizobacteria (PGPR). Here we review the structure and bacterial diversity of the rhizosphere. The major points discussed here are: (1) structure and composition of the rhizosphere (2) range of bacteria found in rhizosphere and their interactions with the plant with a particular emphasis on PGPR (3) mechanisms of plant growth promotion by the PGPR (4) rhizosphere competence.

Keywords

Sustainable agriculture Rhizosphere Plant growth promoting rhizobacteria Plant–microbe interactions 
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References

  1. Ahemad M, Khan MS (2010a) Phosphate-solubilizing and plant-growth-promoting Pseudomonas aeruginosa PS1 improves green gram performance in quizalafop-p-ethyl and clodinafop amended soil. Arch Environ Contam Toxicol 58:361–372Google Scholar
  2. Ahemad M, Khan MS (2010b) Influence of selective herbicides on plant growth promoting traits of phosphate solubilizing Enterobacter asburiae strain PS2. Res J Microbiol 5:849–857Google Scholar
  3. Ahemad M, Khan MS (2010c) Insecticide-tolerant and plant-growth-promoting Rhizobium improves the growth of lentil (Lens esculentus) in insecticide-stressed soils. Pest Manag Sci 67:423–429Google Scholar
  4. Ahemad M, Khan MS (2011) Pseudomonas aeruginosa strain PS1 enhances growth parameters of green gram [Vigna radiata (L.) Wilczek] in insecticide-stressed soils. J Pest Sci 84:123–131Google Scholar
  5. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 168:173–181Google Scholar
  6. Akhtar MS, Siddiqui ZA (2009) Use of plant growth-promoting rhizobacteria for the biocontrol of root-rot disease complex of chickpea. Australas Plant Pathol 38:44–50Google Scholar
  7. Aneja KR (2003) Experiments in microbiology, plant pathology and biotechnology. Age International (P) Limited Publishers, New DelhiGoogle Scholar
  8. Antoun H, Prevost D (2005) Ecology of plant growth promoting rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 1–38Google Scholar
  9. Atlas RM, Bartha R (1993) Microbial ecology: fundamentals and applications. Benjamin/Cummings, Redwood CityGoogle Scholar
  10. Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740Google Scholar
  11. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32Google Scholar
  12. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266Google Scholar
  13. Barea JM (2000) Rhizosphere and mycorrhiza of field crops. In: Balazs E, Galante E, Lynch JM, Schepers JS, Toutant JP, Werner D, Werry PJ (eds) Biological resource management: connecting science and policy. Springer, New York, pp 110–125Google Scholar
  14. Bargabus-Larson RL, Jacobsen BJ (2007) Biocontrol elicited systemic resistance in sugar beet is salicylic acid independent and NPR1 dependent. J Sugar Beet Res 44:17–33Google Scholar
  15. Barriuso J, Solano BR, Lucas JA, Lobo AP, Villaraco AG, Manero FJG (2008) Ecology, genetic diversity and screening strategies of plant growth promoting rhizobacteria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant–bacteria interactions: strategies and techniques to promote plant growth. Wiley-VCH Verlag GmbH and Co. KGaA, Weinheim, pp 1–17Google Scholar
  16. Belimov AA, Kojemiakov AP, Chuvarliyeva CV (1995) Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant Soil 173:29–37Google Scholar
  17. Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz K, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652Google Scholar
  18. Berg G (2000) Diversity of antifungal and plant-associated Serratia plymuthica strains. J Appl Microbiol 88:952–960Google Scholar
  19. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18Google Scholar
  20. Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338Google Scholar
  21. Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2005) Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl Environ Microbiol 71:4203–4213Google Scholar
  22. Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56:250–261Google Scholar
  23. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650Google Scholar
  24. Bolton HJ, Fredrickson JK, Elliott LF (1993) Microbial ecology of the rhizosphere. In: Metting FBJ (ed) Soil microbial ecology. Marcel Dekker, New York, pp 27–63Google Scholar
  25. Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503Google Scholar
  26. Bowen G, Rovira A (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102Google Scholar
  27. Brimecombe MJ, de Leij FA, Lynch JM (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinto R, Varanini Z, Nannipierei P (eds) The rhizosphere. Marcel Dekker, New York, pp 95–141Google Scholar
  28. Brophy LS, Heichel GH (1989) Nitrogen release from roots of alfalfa and soybean grown in sand culture. Plant Soil 116:77–84Google Scholar
  29. Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800Google Scholar
  30. Buyer JS, Roberts DP, Russek-Cohen E (2002) Soil and plant effects on microbial community structure. Can J Microbiol 48:955–964Google Scholar
  31. Cadena MB, Burelle NK, Lawrence KS, van Santen E, Kloepper JW (2008) Suppressiveness of root-knot nematodes mediated by rhizobacteria. Biol Control 47:55–59Google Scholar
  32. Cameron RK, Dixon R, Lamb C (1994) Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J 5:715–725Google Scholar
  33. Cawoy H, Bettiol W, Fickers P, Ongena M (2011) Bacillus based biological control of plant diseases. In: Stoytcheva M (ed) Pesticides in the modern world—pesticides use and management. InTech, Rijeka, pp 273–302Google Scholar
  34. Chaiharn M, Chunhaleuchanon S, Lumyong S (2009) Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World J Microbiol Biotechnol 25:1919–1928Google Scholar
  35. Chanway CP, Holl FB (1992) Influence of soil biota on Douglas fir (Pseudotsuga menziesii) seedling growth: the role of rhizosphere bacteria. Can J Bot 70:1025–1031Google Scholar
  36. Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41Google Scholar
  37. Cheng W, Gershenson A (2007) Carbon fluxes in the rhizosphere. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere—an ecological perspective. Academic Press, San Diego, CA, pp 31–56Google Scholar
  38. Clark FE (1949) Soil microorganisms and plant roots. Adv Agron 1:241–288Google Scholar
  39. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Critical Rev Microbiol 21:1–18Google Scholar
  40. Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moenne-Loccoz Y (2009) Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48:505–512Google Scholar
  41. Cullimore DR, Woodbine M (1963) Rhizosphere effect of the pea root on soil algae. Nature 198:304–305Google Scholar
  42. Curl EA, Truelove B (1986) The rhizosphere. Springer, BerlinGoogle Scholar
  43. de Meyer G, Hofte M (1997) Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathology 87:588–593Google Scholar
  44. de Weger LA, van der Vlugt CIM, Wijfjes AHM, Bakker PAHM, Schippers B, Lugtenberg BJJ (1987) Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J Bacteriol 169:2769–2773Google Scholar
  45. de Weger LA, Bakker PAHM, Schippers B, van Loosdrecht MCM, Lugtenberg BJJ (1989) Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharide are affected in their ability to colonize potato roots. In: Lugtenberg BJJ (ed) Signal molecules in plants and plant–microbe interactions. Springer, Berlin, pp 197–202Google Scholar
  46. Elad Y, Chet I (1987) Possible role of competition for nutrients in biocontrol of Pythium damping off by bacteria. Phytopathology 77:90–195Google Scholar
  47. Fang M, Kremer RJ, Motavalli PP, Davis G (2005) Bacterial diversity of rhizospheres of non-transgenic and transgenic corn. Appl Environ Microbiol 71:4132–4136Google Scholar
  48. Farrar J, Hawes M, Jones D et al (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837Google Scholar
  49. Fernandez LA, Zalba P, Gomez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under green house conditions. Biol Fertil Soils 43:803–805Google Scholar
  50. Fischer SE, Fischer SI, Magris S, Mori GB (2006) Isolation and characterization of bacteria from the rhizosphere of wheat. World J Microbiol Biotechnol 23:895–903Google Scholar
  51. Foster RC (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6:189–203Google Scholar
  52. Frankenberger WTJ, Arshad M (1995) Phytohormones in soil: microbial production and function. Dekker, New YorkGoogle Scholar
  53. Fridlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a β-1, 3 glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221Google Scholar
  54. Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270Google Scholar
  55. Garland JL (1996) Patterns of potential C source utilization by rhizosphere communities. Soil Biol Biochem 36:489–498Google Scholar
  56. Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int J Biol Life Sci 1:35–40Google Scholar
  57. Gillis M, Kersters K, Hoste B, Janssens D, Kroppenstedt RM, Stephan MP, Teixeira KRS, Dobereiner J, de Ley J (1989) Acetobacter diazotrophicus sp. nov., a nitrogen fixing acetic acid bacterium associated with sugarcane. Int J Syst Bacteriol 39:361–364Google Scholar
  58. Glick BR (1995) The enhancement of plant growth promotion by free living bacterial. Can J Microbiol 41:109–117Google Scholar
  59. Gobat JM, Aragno M, Matthey W (2004) The living soil: fundamentals of soil science and soil biology. Science Publishers, USAGoogle Scholar
  60. Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendona-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766Google Scholar
  61. Gow NAR, Campbell TA, Morris BM, Osborne MC, Reid B, Shepherd SJ, van West P (1999) Signals and interaction between phytopathogenic zoospores and plant roots. In: England R, Hobbs G, Bainton N, Roberts DMCL (eds) Microbial signaling and communication. University Press, Cambridge, pp 285–305Google Scholar
  62. Granero FM, Capdevila S, Contreras MS, Martyn M, Rivilla R (2005) Two site-specific recombinases are implicated in phenotypic variation and competitive rhizosphere colonization in Pseudomonas fluorescens. Microbiol 151:975–983Google Scholar
  63. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412Google Scholar
  64. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56Google Scholar
  65. Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378Google Scholar
  66. Greenberg BM, Huang XD, Gerwing P, Yu XM, Chang P, Wu SS, Gerhardt K, Nykamp J, Lu X, Glick B (2008) Phytoremediation of salt impacted soils: greenhouse and the field trials of plant growth promoting rhizobacteria (PGPR) to improve plant growth and salt phytoaccumulation. In: Proceeding of the 33rd AMOP technical seminar on environmental contamination and response. Environment Canada, Ottawa, ON, pp 627–637Google Scholar
  67. Hadfield W (1960) Rhizosphere effect on soil algae. Nature 185:179–180Google Scholar
  68. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319Google Scholar
  69. Hiltner L (1904) About new experiences and problems in the field of Bodenbakteriologie. Works Ger Agric Soc 98:59–78Google Scholar
  70. Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303Google Scholar
  71. Hu X, Li W, Chen Q, Yang Y (2009) Early signal transduction linking the synthesis of jasmonic acid in plant. Plant Signal Behav 4:696–697Google Scholar
  72. Huang CJ, Wang TK, Chung SC, Chen CY (2005) Identification of an antifungal chitinase from a potential biocontrol agent, Bacillus cereus 28-9. J Biochem Mol Biol 38:82–88Google Scholar
  73. Hwang BK, Ahn SJ, Moon SS (1994) Production, purification and antifungal activity of the antibiotic nucleoside, tubercidin, produced by Streptomyces violaceoniger. Can J Bot 72:480–485Google Scholar
  74. Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010) Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biol Biochem 42:567–575Google Scholar
  75. Igual JM, Valverde A, Cervantes E, Velazquez E (2001) Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21:561–568Google Scholar
  76. Jaeger JH, Lindow SE, Miller S, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl Environ Microbiol 65:2685–2690Google Scholar
  77. Jangu OP, Sindhu SS (2011) Differential response of inoculation with indole acetic acid producing Pseudomonas sp. in green gram (Vigna radiata L.) and black gram (Vigna mungo L.). Microbiol J 1:159–173Google Scholar
  78. Jayaprakashvel M, Muthezhilan R, Srinivasan R, Hussain JA, Gobalakrishnan S, Bhagat J, Kaarthikeyan C, Muthulakshmi R (2010) Hydrogen cyanide mediated biocontrol potential of Pseudomonas sp. AMET1055 isolated from the rhizosphere of coastal sand dune vegetation. Adv Biotech 9:39–42Google Scholar
  79. Jeffery S, Gardi C, Jones A, Montanarella L, Marmo L, Miko L, Ritz K, Peres G, Roombke J, van der Putten WH (eds) (2010) The soil environment. In: European atlas of soil biodiversity, European Commission, Publications office of the European Union, Luxembourg, pp 17–48Google Scholar
  80. Jeon JS, Lee SS, Kim HY, Ahn TS, Song HG (2003) Plant growth promotion in soil by some inoculated microorganisms. J Microbiol 41:271–276Google Scholar
  81. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480Google Scholar
  82. Joshi P, Bhatt AB (2010) Diversity and function of plant growth promoting rhizobacteria associated with wheat rhizosphere in north Himalayan region. Int J Environ Sci 1:1135–1144Google Scholar
  83. Joshi P, Tyagi V, Bhatt AB (2011) Characterization of rhizobacteria diversity isolated from Oryza sativa cultivated at different altitude in north Himalaya. Adv Appl Sci Res 2:208–216Google Scholar
  84. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35:323–331Google Scholar
  85. Katznelson H, Lochhead AG, Timonin MI (1948) Soil microorganisms and the rhizosphere. Botan Rev 14:543–587Google Scholar
  86. Kim PI, Bai H, Bai D, Chae H, Chung S, Kim Y, Park R, Chi YT (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97:942–949Google Scholar
  87. Kloepper JW (1994) Plant growth-promoting rhizobacteria (other systems). In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, FL, USA, pp 111–118Google Scholar
  88. Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In: Gilbert C (ed) Proceedings 4th international conference on plant pathogenic bacteria, Tours, France, pp 879–882Google Scholar
  89. Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 315–326Google Scholar
  90. Kloepper JW, Ubana RR, Zehnder GW, Murphy JF, Sikora E, Fernandez C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Aust Plant Pathol 28:21–26Google Scholar
  91. Kochian L, Pineros M, Hoekenga O (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195Google Scholar
  92. Koo SY, Cho KS (2009) Isolation and characterization of a plant growth-promoting rhizobacterium, Serratia sp. SY5. J Microbiol Biotechnol 19:1431–1438Google Scholar
  93. Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S, Bonkowski M (2006) Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biol Biochem 38:1665–1672Google Scholar
  94. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371Google Scholar
  95. Lynch JM (1987) The rhizosphere. Wiley Interscience, ChichesterGoogle Scholar
  96. Lynch JM (1990) Some consequences of microbial rhizosphere competence for plant and soil. In: Lynch JM (ed) The rhizosphere. Wiley Interscience, New York, pp 1–10Google Scholar
  97. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10Google Scholar
  98. MacDonald LM, Paterson E, Dawson LA, McDonald AJS (2004) Short-term effects of defoliation on the soil microbial community associated with two contrasting Lolium perenne cultivars. Soil Biol Biochem 36:489–498Google Scholar
  99. Maurhofer M, Keel C, Haas D, Defago G (1994) Pyoluteorin production by Pseudomonas fluorescens strain CHA0 is involved in the suppression of Pythium damping-off of cress but not of cucumber. Eur J Plant Pathol 100:221–232Google Scholar
  100. Maurhofer M, Reimann C, Sacherer SP, Heebs S, Haas D, Defago G (1998) Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against necrosis virus. Phytopathology 88:678–684Google Scholar
  101. Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent Pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624Google Scholar
  102. Morgan JAW, Whipps JM (2001) Methodological approaches to the study of rhizosphere carbon flow and microbial population dynamics. In: Pinton A, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 373–409Google Scholar
  103. Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739Google Scholar
  104. Murphy JF, Zehnder GW (2000) Plant growth-promoting rhizobacterial mediated protection in tomato against tomato mottle virus. Plant Dis 84:779–784Google Scholar
  105. Naik PR, Raman G, Narayanan KB, Sakthivel N (2008) Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiol 8:230–243Google Scholar
  106. Nandakumar R, Babu S, Raguchander T, Samiyappan R (2007) Chitinolytic activity of native Pseudomonas fluorescens strains. J Agri Sci Technol 9:61–68Google Scholar
  107. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2007) Microbial diversity and microbial activity in the rhizosphere. Ciencia del Suelo (Argentina) 25:89–97Google Scholar
  108. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396Google Scholar
  109. Nie M, Zhang XD, Wang JQ et al (2009) Rhizosphere effects on soil bacterial abundance and diversity in the Yellow river deltaic ecosystem as influenced by petroleum contamination and soil salinization. Soil Biol Biochem 41:2535–2542Google Scholar
  110. Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–293Google Scholar
  111. Nowak J (1998) Benefits of in vitro ‘‘biotization’’ of plant tissue cultures with microbial inoculants. In vitro Cell Dev Biol Plant 34:122–130Google Scholar
  112. Parmar N, Dufresne J (2011) Beneficial interactions of plant growth promoting rhizosphere microorganisms. In: Singh A et al (eds) Bioaugmentation, biostimulation and biocontrol, soil biology, vol 28. Springer, Berlin, pp 27–42Google Scholar
  113. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610Google Scholar
  114. Phillips DA, Fox TC, King MD, Bhuvaneswar TV, Teuber LR (2004) Microbial products trigger amino acids exudation from plant roots. Plant Physiol 136:2887–2894Google Scholar
  115. Phillips DA, Fox TC, Six J (2006) Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Global Change Biol 12:561–567Google Scholar
  116. Pinton R, Varanini Z, Nannipieri P (2001) The rhizosphere as a site of biochemical interactions among soil components, plants and microorganisms. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 1–17Google Scholar
  117. Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842Google Scholar
  118. Rawat S, Izhari A, Khan A (2011) Bacterial diversity in wheat rhizosphere and their characterization. Adv Appl Sci Res 2:351–356Google Scholar
  119. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339Google Scholar
  120. Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S, Dhakephalkar PK, Chopade BA (2011) Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J Microbiol Biotechnol 21:556–566Google Scholar
  121. Rouatt JW, Katznelson H, Payne TMB (1960) Statistical evaluation of the rhizosphere effect. Soil Sci Soc Amer Proc 24:271–273Google Scholar
  122. Rougier M, Chaboud A (1989) Biological functions of mucilages secreted by roots. Symp Soc Exp Biol 43:449–454Google Scholar
  123. Rovira AD (1956) Plant root excretions in relation to the rhizosphere effect I. Plant Soil 7:178–194Google Scholar
  124. Sahu GK, Sindhu SS (2011) Disease control and plant growth promotion of green gram by siderophore producing Pseudomonas sp. Res J Microbiol 6:735–749Google Scholar
  125. Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, van Elsas D, Faure JD, Reiter B, Glick BR, Pruski GW, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Sys Evol Microbiol 55:1187–1192Google Scholar
  126. Shetty KG, Hetrick BAD, Figge DAH, Schwab AP (1994) Effects of mycorrhizae and other soil microbes on revegetation of heavy metal contaminated mine spoil. Environ Poll 86:181–188Google Scholar
  127. Slusarenko AJ, Epperlein M, Wood RKS (1983) Agglutination of plant pathogenic and certain other bacteria by pectic polysaccharides from various plant species. Phytopathology 106:337–343Google Scholar
  128. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751Google Scholar
  129. Smit G, Kijne JW, Lugtenberg BJJ (1986) Correlation between extracellular fibrils and attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol 168:821–827Google Scholar
  130. Sobral JK, Araujo WL, Mendes R, Geraldi IO, Kleiner AAP, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251Google Scholar
  131. Soltani AA, Khavazi K, Rahmani HA, Omidvari M, Dahaji PA, Mirhoseyni H (2010) Plant growth promoting characteristics in some Flavobacterium spp. isolated from soils of Iran. J Agri Sci 2:106–115Google Scholar
  132. Steer J, Harris JA (2000) Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32:869–878Google Scholar
  133. Teixeira LCRS, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001Google Scholar
  134. Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170:3499–3508Google Scholar
  135. Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK, Nautiyal CS, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136–150Google Scholar
  136. Trevors JT, van Elas JD (1997) Microbial interaction in soil. In: van Elas JD, Trevars JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker, New York, pp 215–243Google Scholar
  137. Uren NC (2001) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 19–40Google Scholar
  138. van Loon LC (2007) Plant responses to plant growth promoting bacteria. Eur J Plant Pathol 119:243–254Google Scholar
  139. Velineni S, Brahmaprakash GP (2011) Survival and phosphate solubilizing ability of Bacillus megaterium in liquid inoculants under high temperature and desiccation stress. J Agr Sci Tech 13:795–802Google Scholar
  140. Vesper SJ (1987) Production of pili (fimbriae) by Pseudomonas fluorescens and correlation with attachment to corn roots. Appl Environ Microbiol 53:1397–1405Google Scholar
  141. Vesper SJ, Bauer WD (1986) Role of pili (fimbriae) in attachment of Bradyrhizobium japonicum to soybean roots. Appl Environ Microbiol 52:134–141Google Scholar
  142. Viveros OM, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319Google Scholar
  143. Wacquant JP, Ouknider M, Jacquard P (1989) Evidence for a periodic excretion of nitrogen by roots of grass-legume associations. Plant Soil 116:57–68Google Scholar
  144. Wei G, Kloepper JW, Tuzun S (1996) Induced systemic resistance to cucumber diseases and increased plant growth by plant growth promoting rhizobacteria under field conditions. Phytopathology 86:221–224Google Scholar
  145. Weishuang Z, Yingheng FEI, Yi H (2009) Soluble protein and acid phosphatase exuded by ectomycorrhizal fungi and seedlings in response to excessive Cu and Cd. J Environ Sci 21:1667–1672Google Scholar
  146. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407Google Scholar
  147. Whipps JM (1990) Carbon economy. In: Lynch JM (ed) The rhizosphere. Wiley and Son, Chichester, UK, pp 59–87Google Scholar
  148. Whipps JM, Lynch JM (1985) Energy losses by the plant in rhizodeposition. Ann Proceedings Phytochem J Eur 26:59–71Google Scholar
  149. Zehnder G, Kloepper JW, Yao C, Wei G (1997) Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth-promoting rhizobacteria. J Econ Entomol 90:391–396Google Scholar
  150. Zhu F, Qu L, Hong X, Sun X (2011) Isolation and characterization of a phosphate-solubilizing halophilic bacterium Kushneria sp. YCWA18 from Daqiao Saltern on the coast of yellow sea of China. J Evid Based Complement Altern 2011:1–6Google Scholar
  151. Zwart KB, Kuikman PJ, van Veen JA (1994) Rhizosphere protozoa: their significance in nutrient dynamics. In: Darbyshire JF (ed) Soil protozoa. CAB International, Wallingford, pp 93–122Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Pratibha Prashar
    • 1
    • 2
  • Neera Kapoor
    • 1
  • Sarita Sachdeva
    • 2
  1. 1.School of SciencesIGNOUNew DelhiIndia
  2. 2.Department of BiotechnologyFET, MRIUFaridabadIndia

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