Plant Growth Promoting Rhizobacteria and Sustainable Agriculture

  • Azeem Khalid
  • Muhammad Arshad
  • Baby Shaharoona
  • Tariq Mahmood
Chapter

Abstract

The diverse groups of bacteria in close association with roots and capable of stimulating plant growth by any mechanism(s) of action are referred to as plant growth-promoting rhizobacteria (PGPR). They affect plant growth and development directly or indirectly either by releasing plant growth regulators (PGRs) or other biologically active substances, altering endogenous levels of PGRs, enhancing availability and uptake of nutrients through fixation and mobilization, reducing harmful effects of pathogenic microorganisms on plants and/or by employing multiple mechanisms of action. Recently, PGPR have received more attention for use as a biofertilizer for the sustainability of agro-ecosystems. Selection of efficient PGPR strains based on well-defined mechanism(s) for the formulation of biofertilizers is vital for achieving consistent and reproducible results under field conditions. Numerous studies have suggested that PGPR-based biofertilizers could be used as effective supplements to chemical fertilizers to promote crop yields on sustainable basis. Various aspects of PGPR biotechnology are reviewed and discussed.

References

  1. Abou-Shanab RI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889Google Scholar
  2. Abou-Shanab RI, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224Google Scholar
  3. Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). Int J Agri Biol 10:85–88Google Scholar
  4. Ahmad R, Arshad M, Khalid A, Zahir ZA (2008) Effectiveness of organic-/bio-fertilizer supplemented with chemical fertilizers for improving soil water retention, aggregate stability, growth and nutrients uptake of maize (Zea mays L.). J Sust Agri 31:57–77Google Scholar
  5. Ahmed A, Hasnain S (2008) Auxin producing Bacillus sp.: auxin quantification and effect on the growth of Solanum tuberosum. J Biotechnol 136:766–767Google Scholar
  6. Akhtar MJ, Arshad M, Khalid A, Mehmood MH (2005) Substrate-dependent biosynthesis of ethylene by rhizosphere soil fungi and its influence on etiolated pea seedlings. Pedobiologia 49:211–219Google Scholar
  7. Almonacid S, Quintero N, Martinez M, Vela M (2000) Determination of quality parameters of bacterial inocula based on liquid formulation elaborated with strains producing indole acetic acid (IAA). Auburn university websitehttp://www.ag.auburn.edu/argentina/pdfmanuscript/almonacid.pdf
  8. Amor FMD, Martínez AS, Fortea MI, Legua P, Delicado EN (2008) The effect of plant-associative bacteria (Azospirillum and Pantoea) on the fruit quality of sweet pepper under limited nitrogen supply. Sci Hortic 117:191–196Google Scholar
  9. Arshad M, Frankenberger WT Jr (1998) Plant growth regulating substances in the rhizosphere: microbial production and functions. Adv Agron 62:146–151Google Scholar
  10. Arshad M, Frankenberger WT Jr (2002) Ethylene: agricultural sources and applications. Kluwer Academic, New YorkGoogle Scholar
  11. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362PubMedGoogle Scholar
  12. Arshad M, Khalid A (2008) Annual report. University of Agriculture, Faisalabad, PakistanGoogle Scholar
  13. Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with plant growth promoting rhizobacteria containing ACC-deaminase partially eliminates the effects of water stress on growth, yield and ripening of Pisum sativum L. Pedosphere 18:611–620Google Scholar
  14. Asghar HN, Zahir ZA, Arshad M, Khaliq A (2002) Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils 35:231–237Google Scholar
  15. Aslantas R, Cakmakci R, Sahin F (2007) Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Scientia Hort 111:371–377Google Scholar
  16. Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781Google Scholar
  17. Banchio E, Bogino PC, Zygadlo J, Giordano W (2008) Plant growth promoting rhizobacteria improve growth and essential oil yield in Origanum majorana L. Biochem Syst Ecol 36:766–771Google Scholar
  18. Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans Strain PsJN. Appl Environ Microbiol 72:7246–7252Google Scholar
  19. Belimov AA, Dietz KJ (2000) Effect of associative bacteria on element composition of barley seedlings grown in solution culture at toxic cadmium concentrations. Microbiol Res 155:113–21PubMedGoogle Scholar
  20. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250Google Scholar
  21. Belimov AA, Safronova VI, Mimura T (2002) Response of spring rape (Brassica napus var. oleifera L.) to inoculation with plant growth promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase depends on nutrient status of the plant. Can J Microbiol 48:189–199PubMedGoogle Scholar
  22. Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:242–252Google Scholar
  23. Bensalim S, Nowak J, Asiedu SK (1998) A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. J Potato Res 75:145–152Google Scholar
  24. Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886Google Scholar
  25. Blaha D, Prigent-Combaret C, Mirza MS, Moenne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminaseencoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470PubMedGoogle Scholar
  26. Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245PubMedGoogle Scholar
  27. Çakmakçi R, Dönmez F, Aydm A, Şahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487Google Scholar
  28. 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
  29. Cheng Z, Park E, Glick BR (2007) 1-Aminocyclopropane-1-carboxylate (ACC) deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918PubMedGoogle Scholar
  30. Contesto C, Desbrosses G, Lefoulon C, Bena G, Borel F, Galland M, Gamet L, Varoquaux F, Touraine B (2008) Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci 175:178–189Google Scholar
  31. Dazzo FB, Yanni YG, Rizk R, DeBruijn FJ, Rademaker J, Squartini A, Corich V, Mateos P, Martinez-Molina E (2000) Progress in multinational colaboraive studies on the beneficial association between Rhizobium leguminoserum bv. Trifolii and rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. IRRI, Los Banos, pp 167–189Google Scholar
  32. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84Google Scholar
  33. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394PubMedGoogle Scholar
  34. Dodd IC, Belimov AA, Sobeih WY, Safronova VI, Grierson D, Davies WJ (2005) Will modifying plant ethylene status improve plant productivity in water-limited environments? Fourth international crop science congresshttp://www.cropscience.org.au/icsc2004/poster/1/3/4/510_doddicref.htm. Accessed 17 June 2007
  35. Domenech J, Solano BR, Probanza A, Garcıa JAL, Colon JJ, Gutierrez-Manero FJ (2004) Bacillus spp. and Pisolithus tinctorius effects on Quercus ilex ssp. ballota: a study on tree growth, rhizosphere community structure and mycorrhizal infection. Forest Ecol Manage 194:293–303Google Scholar
  36. Donate-Correa J, Leon-Barrios M, Perez-Galdona R (2005) Screening for plant growth-promoting rhizobacteria in Chamaecytisus proliferus (tagasaste), a forage tree-shrub legume endemic to the Canary Islands. Plant Soil 266:261–272Google Scholar
  37. Egamberdiyeva D, Hflich G (2004) Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semiarid region of Uzbekistan. J Arid Environ 56:293–301Google Scholar
  38. Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 24:1187–1193Google Scholar
  39. Frankenberger WT Jr, Arshad M (1995) Phytohormones in soils: microbial production and function. Marcel Dekker, New YorkGoogle Scholar
  40. Garci’a JL, Probanza A, Ramos B, Manero FG (2003) Effects of three plant growth-promoting rhizobacteria on the growth of seedlings of tomato and pepper in two different sterilized and nonsterilized peats. Arch Agron Soil Sci 49:119–127Google Scholar
  41. Glick BR (1995) The enhancement of plant growth by free living bacteria. Can J Microbiol 41:109–117Google Scholar
  42. Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393PubMedGoogle Scholar
  43. Glick BR (2004) Teamwork in phytoremediation. Nature Biotechnol 22:526–527Google Scholar
  44. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7PubMedGoogle Scholar
  45. Glick BR (2006) Plant responses to ACC deaminase-containing PGPR. 7th international workshop on plant growth promoting rhizobacteria, 28 May–2 June 2006. Noordwijkerhout, The Netherlands, p 30Google Scholar
  46. Glick BR, Penrose DM, Li J (1998) A model for lowering plant ethylene concentration by plant growth promoting rhizobacteria. J Theor Biol 190:63–68PubMedGoogle Scholar
  47. Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977Google Scholar
  48. 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
  49. Grichko VP, Glick BR (2001) Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35 S, rolD or PRB-1b promoter. Plant Physiol Biochem 39:19–25Google Scholar
  50. Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, Zhang LX, Sun PH (2004) Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biol Control 29:66–72Google Scholar
  51. Hafeez FY, Yasmin S, Ariani D, Mehboob-ur-Rahman ZY, Malik KA (2006) Plant growth-promoting bacteria as biofertilizer. Agron Sust Dev 26:143–150Google Scholar
  52. Hallberg KB, Johnson DB (2005) Microbiology of a wetland ecosystem constructed to remediate mine drainage from a heavy metal mine. Sci Total Environ 338:53–66PubMedGoogle Scholar
  53. Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) Responses of three grass species to creosote during phytoremediation. Environ Pollut 130:453–63PubMedGoogle Scholar
  54. Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2005) Responses of hydrocarbons (TPHs) from soils. Microchem J 81:139–47Google Scholar
  55. Jeun YC, Park KS, Kim CH, Fowler WD, Kloepper JW (2004) Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biol Control 29:34–42Google Scholar
  56. Jha MN, Prasad AN (2006) Efficacy of new inexpensive cyanobacterial biofertilizer including its shelf-life. World J Microbiol Biotechnol 22:73–79Google Scholar
  57. Kamnev AA, Tugarova AV, Antonyuk LP, Tarantilis PA, Polissiou MG, Gardiner PHE (2005) Effects of heavy metals on plant-associated rhizobacteria: comparison of endophytic and non-endophytic strains of Azospirillum brasilense. J Trace Elem Med Biol 19:91–5PubMedGoogle Scholar
  58. Kao PH, Huang CC, Hseu ZY (2006) Response of microbial activities to heavy metals in a neutral loamy soil treated with biosolid. Chemosphere 64:63–70PubMedGoogle Scholar
  59. Karadeniz A, Topcuoglu SF, Inan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22:1061–1064Google Scholar
  60. Kennedy IR, Choudhury ATMA, Kecskés ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol Biochem 36:1229–1244Google Scholar
  61. Khalequzaman KM, Hossain I (2008) Effect of seed treatment with Rhizobium strains and biofertilizers on foot/root rot and yield of bushbean in Fusarium oxysporum infested soil. J Agric Res 46:55–64Google Scholar
  62. Khalid A, Arshad M, Zahir ZA (2004a) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480PubMedGoogle Scholar
  63. Khalid A, Tahir S, Arshad M, Zahir ZA (2004b) Relative efficiency of rhizobacteria for auxin biosynthesis in rhizosphere vs. non-rhizosphere soil. Aust J Soil Res 42:921–926Google Scholar
  64. Khalid A, Arshad M, Zahir ZA (2006) Phytohormones: microbial production and applications. In: Uphoff N et al (eds) Biological approaches to sustainable soil systems. Taylor & Francis, Boca Raton, Florida, pp 207–220Google Scholar
  65. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364PubMedGoogle Scholar
  66. Khan MS, Zaidi A, Wani PA (2007) Role of phosphate solubilizing microorganisms in sustainable agriculture: a review. Agron Sustain Dev 27:29–43Google Scholar
  67. Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19Google Scholar
  68. Kloepper JW, Scher FM, Tripping B (1986) Emergence promoting rhizobacteria: description and implication for agriculture. In: Swinburne TR (ed) Iron, siderophores and plant diseases. Plenum, New York, pp 155–164Google Scholar
  69. Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252Google Scholar
  70. Kumar B, Trivedi P, Pandey A (2007) Pseudomonas corrugata: a suitable bacterial inoculant for maize grown under rainfed conditions of Himalayan region. Soil Biol Biochem 39:3093–3100Google Scholar
  71. Ladha JK, Reddy PM (2000) The quest for nitrogen fixation in rice. IRRI, Los BanosGoogle Scholar
  72. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522PubMedGoogle Scholar
  73. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25PubMedGoogle Scholar
  74. Madhaiyan M, Suresh Reddy BV, Anandham R, Senthilkumar M, Poonguzhali S, Sundaram SP, Sa TM (2006) Plant growth promoting Methylobacterium induces defense responses in groundnut (Arachis hypogaea L.) compared to rot pathogens. Curr Microbiol 53:270–276PubMedGoogle Scholar
  75. Masoud A, Abbas ST (2009) Evaluation of fluorescent pseudomonads for plant growth promotion, antifungal activity against Rhizoctonia solani on common bean, and biocontrol potential. Biol Control 48:101–107Google Scholar
  76. Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci 166:525–530Google Scholar
  77. Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedGoogle Scholar
  78. Mayak S, Tivosh T, Glick BR (1999) Effect of wild type and mutant plant growth-promoting rhizobacteria on the rooting of mungbeen cuttings. J Plant Growth Regul 18:49–53PubMedGoogle Scholar
  79. Mena-Violante HG, Olalde-Portugal V (2007) Alteration of tomato fruit quality by root inoculation with plant growth-promoting rhizobacteria (PGPR): Bacillus subtilis BEB-13bs. Sci Hortic 113:103–106Google Scholar
  80. Mirik M, Aysan Y, Cinar O (2008) Biological control of bacterial spot disease of pepper with Bacillus strains. Turk J Agri For 32:381–390Google Scholar
  81. Mubeen F, Aslam A, Radl V, Schloter M, Malik KA, Hafeez FY (2008) Role of nature’s fertility partners with crop protectants for sustainable agriculture. In: Dakora FD et al (eds) Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Springer, The Netherlands, pp 153–154Google Scholar
  82. Muratova AY, Turkovskaya OV, Antonyuk LP, Makarov OE, Pozdnyakova LI, Ignatov VV (2005) Oil-oxidizing potential of associative rhizobacteria of the genus Azospirillum. Microbiol 74:210–215Google Scholar
  83. Nadeem SM, Zahir ZA, Naveed M, Arshad M, Shahzad SM (2006) Variation in growth hizobacteand ion uptake of maize due to inoculation with plant growth promoting rria under salt stress. Soil Environ 25:78–84Google Scholar
  84. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC-deaminase activity. Can J Microbiol 53:1141–1149PubMedGoogle Scholar
  85. Naiman AD, Latronico A, Garcıa de Salamone IE (2009) Inoculation of wheat with Azospirillum brasilense and Pseudomonas fluorescens: impact on the production and culturable rhizosphere microflora. Eur J Soil Biol 45:44–51Google Scholar
  86. Nakkeeran S, Fernando WGD, Siddiqui A (2005) Plant growth promoting rhizobacteria formulations and its scope in commercialization for the management of pests and diseases. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, The Netherlands, pp 257–296Google Scholar
  87. Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–53PubMedGoogle Scholar
  88. Narayanasamy P (2008) Molecular biology in plant pathogenesis and disease management. Springer, The NetherlandsGoogle Scholar
  89. 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
  90. Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111:38–43Google Scholar
  91. Pandey P, Kang SC, Maheshwari DK (2005) Isolation of endophytic plant growth promoting Burkholderia sp. MSSP from root nodules of Mimosa pudica. Curr Sci 89:170–180Google Scholar
  92. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220PubMedGoogle Scholar
  93. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801PubMedGoogle Scholar
  94. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15PubMedGoogle Scholar
  95. Pishchik VN, Vorobyev NI, Chernyaeva II, Timofeeva SV, Kozhemyakov AP, Alexeev YV, Lukin SM (2002) Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant Soil 243:173–186Google Scholar
  96. Poi SC, Kabi MC (1979) Effect of Azotobacter inoculation on growth and yield of jute and wheat. Indian J Agri Sci 49:478–480Google Scholar
  97. Probanza A, Garcıa JAL, Palomino MR, Ramos B, Mañero FJG (2002) Pinus pinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CECT 5,106 and B. pumilus CECT 5,105). Appl Soil Ecol 20:75–84Google Scholar
  98. Raj SN, Deepak SA, Basavaraju P, Shetty HS, Reddy MS, Kloepper JW (2003) Comparative performance of formulations of plant growth promoting rhizobacteria in growth promotion and suppression of downy mildew in pearl millet. Crop Prot 22:579–88Google Scholar
  99. Rasche F, Velvis H, Zachow C, Berg G, Van Elsas JD, Sessitsch A (2006) Impact of transgenic potatoes expressing anti-bacterial agents on bacterial endophytes is comparable with the effects of plant genotype, soil type and pathogen infection. J Appl Ecol 43:555–566Google Scholar
  100. Reed MLE, Warner BG, Glick BR (2005) Plant growth-promoting bacteria facilitate the growth of the common reed Phragmites australis in the presence of copper or polycyclic aromatic hydrocarbons. Curr Microbiol 51:425–429PubMedGoogle Scholar
  101. Römkens P, Bouwman L, Japenga J, Draaisma C (2002) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ Pollut 116:109–121PubMedGoogle Scholar
  102. Safronova VI, Stepanok VV, Engqvist GL, Alekseyev YV, Belimov AA (2006) Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol Fertil Soils 42:267–272Google Scholar
  103. Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspectives of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Indust Microbiol Biotechnol 34:635–648Google Scholar
  104. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292PubMedGoogle Scholar
  105. Senthilkumar M, Madhaiyan M, Sundaram SP, Kannaiyan S (2009) Intercellular colonization and growth promoting effects of Methylobacterium sp. with plant-growth regulators on rice (Oryza sativa L. Cv CO-43). Microbiol Res 164:92–104PubMedGoogle Scholar
  106. Serdyuk OP, Smolygina LD, Muzafarov EN, Adanin VM, Arinbasarov MU (1995) 4-Hydroxyphenethyl alcohol – a new cytokinin-like substance from the phototrophic purple bacterium Rhodospirillum rubrum 1R. FEBS Lett 365:10–12PubMedGoogle Scholar
  107. Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka E, Wang-Pruski G, Faure D, Reiter B, Glick BR, Nowak J (2005) Burkholderia phytofirmins sp. Nov., a novel plant-associated bacterium with plant beneficial properties. Int J Syst Evol Microbiol 55:1187–1192PubMedGoogle Scholar
  108. Shaharoona B, Arshad M, Zahir ZA, Khalid A (2006a) 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 38:2971–2975Google Scholar
  109. Shaharoona B, Arshad M, Zahir ZA (2006b) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation of mungbean (Vigna radiata). Lett Appl Microbiol 42:155–159PubMedGoogle Scholar
  110. Shaharoona B, Arshad M, Khalid A (2007a) Differential response of etiolated pea seedling to 1-aminocyclopropane-1-carboxylate and/or L-methionine utilizing rhizobacteria. J Microbiol 45:15–20PubMedGoogle Scholar
  111. Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007b) Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.). J Microbiol Biotechnol 17:1300–1307PubMedGoogle Scholar
  112. Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer dependent efficiency of Pseudomonads containing ACC-deaminase for improving growth, yield and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155PubMedGoogle Scholar
  113. Shahzad MS, Khalid A, Arshad M, Khalid M, Mehboob I (2008) Integrated use of plant growth promoting bacteria and P-enriched compost for improving growth, yield and nodulation of chickpea. Pak J Bot 40:1735–1744Google Scholar
  114. Shaukat K, Affrasayab S, Hasnain S (2006) Growth responses of Triticum aestivum to plant growth promoting rhizobacteria used as a biofertilizer. Res J Microbiol 1:330–338Google Scholar
  115. Sheng XF, Xia JJ (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64:1036–1042PubMedGoogle Scholar
  116. Sindhu SS, Gupta SK, Dadarwal KR (1999) Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of plant growth in green gram (Vigna radiata). Biol Fertil Soils 29:62–68Google Scholar
  117. Sindhu SS, Suneja S, Goel AK, Parmar N, Dadarwal KR (2002) Plant growth promoting effects of Pseudomonas sp. on coinoculation with Mesorhizobium sp. Cicer strain under sterile and “wilt sick” soil conditions. Appl Soil Ecol 19:57–64Google Scholar
  118. Singh B, Kahlon RS, Sahoo SK et al (2005) Residues of lindane and endosulfan in soil and their effect on soil microbial population and dehydrogenase activity. Pesticide Res J 17:88–90Google Scholar
  119. Stiens M, Schneiker S, Keller M, Kuhn S, Pühler A, Schlüter A (2006) Sequence analysis of the 144-kilobase accessory plasmid psmesm11a, isolated from a dominant Sinorhizobium meliloti strain identified during a long-term field release experiment. Appl Environ Microbiol 72:3662–3672PubMedGoogle Scholar
  120. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852Google Scholar
  121. Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AL (2007) Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res 162:69–76PubMedGoogle Scholar
  122. Tuomi T, Rosenquist H (1995) Detection of abscisic, gibberellic and indole-3-acetic acid from plant and microbes. Plant Physiol Biochem 33:725–734Google Scholar
  123. Umrania VV (2006) Bioremediation of toxic heavy metals using acidothermophilic autotrophes. Bioresour Technol 97:1237–1242PubMedGoogle Scholar
  124. Van Loon LC (2007) Plant response to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254Google Scholar
  125. Van Loon LC, Glick BR (2004) Increased plant fitness by rhizobacteria. In: Sandermann H (ed) Molecular ecotoxicology of plants. Springer, Berlin, pp 178–205Google Scholar
  126. Vig K, Singh DK, Sharma PK (2006) Endosulfan and quinalphos residues and toxicity to soil microarthropods after repeated applications in a field investigation. J Environ Sci Health Part B 41:681–692Google Scholar
  127. Villacieros M, Whelan C, Mackova M, Molgaard J, Sanchez-Contreras M, Lloret J (2005) Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl Environ Microbiol 71:2687–2694PubMedGoogle Scholar
  128. Wang CKE, Glick BR, Defago G (20 00) 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 46:898–907PubMedGoogle Scholar
  129. Wani PA, Khan MS, Zaidi A (2007) Co-inoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth yield and nutrient uptake in chickpea. Acta Agron Hung 55:315–323Google Scholar
  130. Wani PA, Khan MS, Zaidi A (2008a) Effect of metal tolerant plant growth promoting Rhizobium on the performance of pea grown in metal amended soil. Arch Environ Contam Toxicol 55:33–42PubMedGoogle Scholar
  131. Wani PA, Khan MS, Zaidi A (2008b) Chromium reducing and plant growth promoting Mesorhizobium improves chickpea growth in chromium amended soil. Biotechnol Lett 30:159–163PubMedGoogle Scholar
  132. 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. Phytopathol 86:221–224Google Scholar
  133. Weingart H, Volksch B, Ullrich MS (1999) Comparison of ethylene production by Pseudomonas syringae and Ralstonia aolanacearum. Phyopathology 89:360–365Google Scholar
  134. Wu SC, Caob ZH, Lib ZG, Cheunga KC, Wonga MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166Google Scholar
  135. Wu SC, Luo YM, Cheung KC, Wong MH (2006) Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ Pollut 144:765–773PubMedGoogle Scholar
  136. Zahir ZA, Abbas SA, Khalid A, Arshad M (2000) Substrate-dependent microbially derived plant hormones for improving growth of maize seedlings. Pak J Biol Sci 3:289–291Google Scholar
  137. Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:96–168Google Scholar
  138. Zahir ZA, Asghar HN, Akhtar MJ, Arshad M (2005) Precursor (l-tryptophan)-inoculum interaction for improving yields and nitrogen uptake of maize. J Plant Nutr 28:805–817Google Scholar
  139. Zahir ZA, Munir A, Asghar HN, Arshad M, Shaharoona B (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:982–987Google Scholar
  140. Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997PubMedGoogle Scholar
  141. Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth promoting rhizobacteria for bioremediation. Environ Int 33:406–413PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • Azeem Khalid
    • 2
  • Muhammad Arshad
    • 1
  • Baby Shaharoona
    • 1
  • Tariq Mahmood
    • 2
  1. 1.Institute of Soil and Environmental Sciences, University of AgricultureFaisalabadPakistan
  2. 2.Department of Environmental Sciences, PMAS Arid Agriculture UniversityRawalpindiPakistan

Personalised recommendations