Advertisement

Plant Growth Promoting Rhizobacteria as Alleviators for Soil Degradation

  • Metin Turan
  • Ahmet Esitken
  • Fikrettin Sahin
Chapter

Abstract

Soil degradation refers to decline in the soil’s productivity through deterioration of its physical, chemical, and biological properties. The most important processes and causes of degradation are water–wind erosion, salinization, alkalinization, acidification, and leaching and soil pollution. The rate of soil degradation is directly related to unsuitable land use. While growers routinely use physical and chemical approaches to manage the soil environment to improve crop yields, the application of microbial products for this purpose is less common. However, plant growth promoting rhizobacteria (PGPRs) can prevent the deleterious effects of one or more stressors from the environment. These beneficial microorganisms can be a significant component of management practices to achieve the attainable yield in degraded soil. In such soils, the natural role of stress-tolerant PGPRs in maintaining soil fertility is more important than in conventional agriculture. Besides their role in metal detoxification/removal, salinization, and acidification, rhizobacteria also promote the growth of plants by other mechanisms such as production of growth promoting substances and siderophores. Remediation with PGPRs is called bioremediation in degraded soil and is another emerging low-cost in situ technology (Cohen et al. Int J Green Energy 3:301–312, 2004) employed to remove or alleviate pollutants, salinity, and acidification stress from the degraded land. The efficiency of bioremediation can be enhanced by the judicious and careful application of appropriate heavy metal, salinity, acidity tolerant, and plant growth promoting rhizobacteria including symbiotic nitrogen-fixing organisms. This review presents the results of studies on the recent developments in the utilization of PGPR for direct application in soils degraded with heavy metals, salinity, and acidity under a wide range of agroecological conditions with a view to restore degraded soils and consequently, promote crop productivity in degraded soils across the globe and their significance in bioremediation.

Keywords

Nitric Oxide Heavy Metal Arbuscular Mycorrhizal Fungus Plant Growth Promote Rhizobacteria Degraded Soil 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abou-Shanab RA, Delorme TA, Angle JS, Chaney RL, Ghanem K, Moawad H (2003) Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int J Phytoremed 5:367–379Google Scholar
  2. Abou-Shanab RA, 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
  3. Alvey S, Crowley DE (1996) Survival and activity of an atrazine-mineralizing bacterial consortium in rhizosphere soil. Environ Sci Technol 30:1596–1603Google Scholar
  4. Antoun H, Prevost D (2006) Ecology of plant growth promoting rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 1–38Google Scholar
  5. Arasimovic M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Sci 172:876–887Google Scholar
  6. Ashraf M, Foolad MR (2007) Roles of glycinebetaine and proline in improving plant abiotic stress tolerance. Environ Exp Bot 59:206–216Google Scholar
  7. Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedling with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:152–157Google Scholar
  8. Baligar VC, Fageria NK (1997) Nutrient use efficiency in acid soils: nutrient management and plant use efficiency. In: Moniz AC (ed) Plant soil ınteractions at low pH. Brazilian Soil Science Society, Vicosa, pp 75–95Google Scholar
  9. Barber SA, Lee RB (1974) The effect of microorganisms on the absorption of manganese by plants. New Phytol 73:97–106Google Scholar
  10. Bashan Y, de Bashan LE (2005) Bacteria/plant growth-promotion. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 103–115Google Scholar
  11. Baudouin C, Charveron M, Tarrouse R, Gall Y (2002) Environmental pollutants and skin cancer. Cell Biol Toxicol 18:341–348PubMedGoogle Scholar
  12. Beinroth FH, Eswaran H, Reich PF, Van Den Berg E (1994) Land related stresses in agroecosystems. In: Virmani SM, Katyal JC, Eswaran H, Abrol IP (eds) Stressed ecosystems and sustainable agriculture. Oxford and IBH, New Delhi, pp 131–148Google Scholar
  13. Belimov AA, Kunakova AM, Safronova VI, Stepanok VV, Yudkin LY, Alekseev YV, Kozhemyakov AP (2004) Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiology (Moscow) 73:99–106Google Scholar
  14. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S (2005) Cadmium-tolerant plant growth-promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250Google Scholar
  15. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39PubMedGoogle Scholar
  16. Birch GE, Scollen A (2003) Heavy metals in road dust, gully pots and parkland soils in a highly urbanised subcatchment of Port Jackson, Australia. Aust J Soil Res 41:1329–1342Google Scholar
  17. 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
  18. Borsani O, Cuartero J, Fermandez JA, Valpuesta V, Botella MA (2001) Identification of two loci in tomato leaves distinct mechanism for salt tolerance. Plant Cell 13:167–179Google Scholar
  19. Brazil GM, Kenefick L, Callanan M, Haro A, de Lorenzo V, Dowling DN (1995) Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated biphenyls and detection of bph gene expression in the rhizosphere. Appl Environ Microbiol 61:1946–1952PubMedGoogle Scholar
  20. Brookes PC, McGrath SP (1984) Effects of metal toxicity on the size of the soil microbial biomass. J Soil Sci 35:341–346Google Scholar
  21. Brown MT, Ulgiati S (1999) Emergy evaluation of natural capital and biosphere services. AMBIO 28(6)Google Scholar
  22. Bruntland GH (ed) (1987) Our common future: the World Commission on Environment and Development. Oxford University Press, OxfordGoogle Scholar
  23. Budzikiewicz H (1997) Siderophores of fluorescent Pseudomonas L. Nat Foresche 52C:413–420Google Scholar
  24. Burd GI, DixonDG DG, Glick BR (1998) A plant growth promoting bacterium that decreases nickel toxicity in plant seedlings. Appl Environ Microbiol 64:3663–3668PubMedGoogle Scholar
  25. 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
  26. Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321Google Scholar
  27. Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284PubMedGoogle Scholar
  28. Chaney RL, Brown SL, Li YM, Angle JS, Stuczynski TI, Daniel WL, Henry CL, Siebelec G, Malik M, Ryan JA (2000) Progress in risk assessment for soil metals, and in-situ remediation and phytoextraction of metals from hazardous contaminated soils. US-EPA “Phytoremediation: State of Science”, Boston, MAGoogle Scholar
  29. Chaudri AM, McGrath SP, Giller KE, Rietz E, Sauerbeck DR (1993) Enumeration of indigenous Rhizobium leguminosarum biovar trifolii in soils previously treated with metal-contaminated sewage sludge. Soil Biol Biochem 25:301–309Google Scholar
  30. Chekol T, Vough LR, Chaney R (2004) Phytoremediation of polychlorinated biphenylcontaminated soils: the rhizosphere effect. Environ Int 30:799–804PubMedGoogle Scholar
  31. Cheng S, Grosse W, Karrenbrock F, Thoennessen M (2002) Efficiency of constructed wetlands in decontamination of water polluted by heavy metals. Ecol Eng 18:317–325Google Scholar
  32. Cohen MF, Yamasaki H, Mazzola M (2004) Bioremediation of soils by plant-microbe systems. Int J Green Energy 3:301–312Google Scholar
  33. Cohen MF, Mazzola M, Yamasaki H (2006) Nitric oxide research in agriculture: bridging the plant and bacterial realms. In: Rai AK, Takabe T (eds) Abiotic stress tolerance in plants. Springer, Dordrecht, pp 71–90Google Scholar
  34. Cohen MF, Lamattina L, Yamasaki H (2010) Nitric oxide signaling by plant-associated bacteria. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley-VCH, Weinheim, pp 161–172Google Scholar
  35. Crowley DE, Wang YC, Reid CPP, Szansiszlo PJ (1991) Mechanism of iron acquisition from siderophores by microorganisms and plants. Plant Soil 130:179–198Google Scholar
  36. Crowley DE, Brennerova ME, Irwin C, Brenner V, Focht DD (1996) Rhizosphere effects on biodegradation of 2,5-dichlorobenzoate by a bioluminescent strain of rootcolonizing Pseudomonas fluorescens. FEMS Microbiol Ecol 20:79–89Google Scholar
  37. Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 158:39–49Google Scholar
  38. Davies FT Jr, Puryear JD, Newton RJ (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J Plant Physiol 158:777–786Google Scholar
  39. Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Ecol 52:153–162PubMedGoogle Scholar
  40. Diaz-Ravina M, Baath E (1996a) Development of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels. Appl Environ Microbiol 62:2970–2977PubMedGoogle Scholar
  41. Diaz-Ravina M, Baath E (1996b) Thymidine and leucine incorporation into bacteria from soils experimentally contaminated with heavy metals. Appl Soil Ecol 3:225–234Google Scholar
  42. Donnelly KP, Hegde SR, Fletcher SH (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–988Google Scholar
  43. Duffy BK, Defago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438PubMedGoogle Scholar
  44. Dugardeyn J, Van Der Straeten D (2008) Ethylene: fine-tuning plant growth and development by stimulation and inhibition of elongation. Plant Sci 175:59–70Google Scholar
  45. Ehret DL, Ho LC (1986) Translocation of calcium in relation to tomato fruit growth. Ann Bot 58:679–688Google Scholar
  46. Ehsanpour AA, Amini F (2003) Effect of salt and drought stress on acid phosphatase activities in alfalfa (Medicago sativa L.) explants under in vitro culture. Afr J Biotechnol 2:133–135Google Scholar
  47. Ellis RJ, Timms-Wilson TM, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ Microbiol 2:274–284PubMedGoogle Scholar
  48. EPA (2000) Introduction to phytoremediation. National Risk Management Research Laboratory, Office of Research and Development, EPA/600/R-99/107 (U.S. Environmental Protection Agency)Google Scholar
  49. Ernst WHO (1996) Bioavailability of heavy metals and decontamination of soil by plants. Appl Geochem 11:163–167Google Scholar
  50. Esty DC, Levy M, Srebotnjak T, de Sherbinin A (2005) Environmental sustainability index: benchmarking national environmental stewardship. Yale Center for Environmental Law and Policy, New HavenGoogle Scholar
  51. FAO (2000) Global network on integrated soil management for sustainable use of salt effected soils. http://www.fao.org/ag/AGL/agll/spush/intro.htm
  52. Fletcher JS, Hedge RS (1995) Release of phenols by perennial plant roots and their potential importance in bioremediation. Chemosphere 31:3009–3016Google Scholar
  53. Fliessbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26:1201–1205Google Scholar
  54. Frostegard A, Tunlid A, Baath E (1993) Phospholipid fatty acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617PubMedGoogle Scholar
  55. Frostegard A, Tunlid A, Baath E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28:55–63Google Scholar
  56. Ghassemi F, Jakeman AJ, Nix HA (1995) Salinization of land water resources. CAB International, Wallingford, UKGoogle Scholar
  57. Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Skarzhinskaya M, Dushenkov S, Logendra S, Gleba YY, Raskin I (1999) Use of plant roots for phytoremediation and molecular farming. Proc Natl Acad Sci USA 96:5973–5977PubMedGoogle Scholar
  58. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117Google Scholar
  59. Glick BR (2001) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393Google Scholar
  60. Glick BR, Liu C, Ghosh S, Dumbrof EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239Google Scholar
  61. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68PubMedGoogle Scholar
  62. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-containing soil bacteria. Eur J Plant Pathol 119:329–339Google 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. Guan LL, Kanoh K, Kamino K (2001) Effect of exogenous siderophores on iron uptake activity of marine bacteria under ironlimited conditions. Appl Environ Microbiol 67:1710–1717PubMedGoogle Scholar
  65. 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
  66. Hamdia MA, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44:165–174Google Scholar
  67. Han HS, Lee KD (2004a) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1:210–215Google Scholar
  68. Han HS, Lee KD (2004b) Physiological responses of soybean- inoculation of Bradyrhzobium japonicum with PGPR in saline soil conditions. Res J Agric Biol Sci 1:216–221Google Scholar
  69. Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) A multiprocess phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ Pollut 130:465–476PubMedGoogle Scholar
  70. Huang XD, El-Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem J 81:139–147Google Scholar
  71. International Institute for Sustainable Development (1996) Global tomorrow coalition sustainable development tool kit: a sample policy framework, Chap. 4. IISD, ManitobaGoogle Scholar
  72. Ipek M, Pirlak L, Esitken A, Donmez MF, Turan M, Sahin F (2011) Plant growth-promoting rhizobacteria (PGPR) increase yield, growth and nutrition of strawberry under high calcareous soil conditions. J Plant Nutr (in process)Google Scholar
  73. Jacobsen CS (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 189:139–144Google Scholar
  74. Kamprath EJ (1984) Crop response to lime in soils in the tropics. In: Adams F (ed) Soil acidity and liming, 2nd edn. Agronomy monograph 9. American Society for Agronomy and Soil Science Society of America, Madison, WI, pp 643–698Google Scholar
  75. 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
  76. Karlidag H, Esitken A, Yildirim E, Donmez MF, Turan M (2011) Effects of plant growth promoting bacteria on yield, growth, leaf water content, membrane permeability and ionic composition of strawberry under saline conditions. J Plant Nutr 34(1):34–45Google Scholar
  77. Kim SO, Moon SH, Kim KW (2001) Removal of heavy metals from soils using enhanced electrokinetic soil processing. Water Air Soil Pollut 125:259–272Google Scholar
  78. Knasmuller S, Gottmann E, Steinkellner H, Fomin A, Pickl C, Paschke A (1998) Detection of genotoxic effects of heavy metal contaminated soils with plant bioassays. Mutat Res 420:37–48PubMedGoogle Scholar
  79. Kohler J, Caravaca F, Carrasco L, Roldan A (2006) Contribution of Pseudomonas mendocina and Glomus intraradices to aggregates stabilisation and promotion of biological properties in rhizosphere soil of lettuce plants under field conditions. Soil Use Manage 22:298–304Google Scholar
  80. Koomen I, McGrath SP, Giller KE (1990) Mycorrhizal infection of clover is delayed in soils contaminated with heavy metals from past sewage sludge applications. Soil Biol Biochem 22:871–873Google Scholar
  81. Kozdroj J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417Google Scholar
  82. Krasylenko YA, Yemets AI, Blume YB (2010) Functional role of nitric oxide in plants. Russ J Plant Physiol 57:451–461Google Scholar
  83. Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 32:2090–2102Google Scholar
  84. Kuznetsov VV, Shevyakova NI (1997) Stress responses of tobacco cells to high temperature and salinity. Proline accumulation and phosphorylation of polypeptides. Physiol Plant 100:320–326Google Scholar
  85. Lal R (1994) Tillage effects on soil degradation, soil resilience, soil quality, and sustainability. Soil Tillage Res 27:1–8Google Scholar
  86. Lasat HA (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120PubMedGoogle Scholar
  87. Lebeau TB, Braud A, Jezequel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522PubMedGoogle Scholar
  88. Lee G, Carrow RN, Duncan RR, Eiteman MA, Rieger MW (2008) Synthesis of organic osmolytes and salt tolerance mechanisms in Paspalum vaginatum. Environ Exp Bot 63:19–27Google Scholar
  89. Lee S-W, Ahn I-P, Sim S-Y, Lee S-Y, Seo M-W, Kim S, Park S-Y, Lee Y-H, Kang S (2010) Pseudomonas sp. LSW25R, antagonistic to plant pathogens, promoted plant growth, and reduced blossom-end rot of tomato fruits in a hydroponic system. Eur J Plant Pathol 126:1–11Google Scholar
  90. Liste HH, Alexander M (2000) Accumulation of phenanthrene and pyrene in rhizosphere soil. Chemosphere 40:11–14PubMedGoogle Scholar
  91. Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336Google Scholar
  92. Lo IMC, Yang XY (1999) EDTA extraction of heavy metals from different soil fractions and synthetic soils. Water Air Soil Pollut 109:219–236Google Scholar
  93. Lodewyckx C, Taghavia S, Mergeaya M, Vangronsveldb J, Clijstersb H, van der Lelie D (2001) The effect of recombinant heavy metal resistant endophytic bacteria on heavy metal uptake by their host plant. Int J Phytoremed 3:173–187Google Scholar
  94. Malik A, Jaiswal R (2000) Metal resistance in Pseudomonas strains isolated from soil treated with industrial wastewater. World J Microbiol Biotechnol 16:177–182Google Scholar
  95. Mayak S, Tirash T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedGoogle Scholar
  96. McEldowney S, Hardman DJ, Waite S (1993) Treatment technologies. In: McEldowney S, Hardman DJ, Waite S (eds) Pollution, ecology and biotreatment. Longman Singapore, Singapore, pp 48–58Google Scholar
  97. Meyer JM (2000) Pyoverdines: pigments siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol 174:135–142PubMedGoogle Scholar
  98. Miller RR (1996) Phytoremediatian. Technology Overview Report, TO-96-03. Ground-Water Remediation Technology Analysis Center, PittsburghGoogle Scholar
  99. Molina-Favero C, Creus CM, Lanterı ML, Correa-Aragunde N, Lombardo MC, Barassi CA, Lamattina L (2007) Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv Bot Res 46:1–33Google Scholar
  100. Murillo-Amador B, Jones HG, Kaya C, Aguilar RL, Garcia-Hernandez JL, Troyo-Dieguez E, Avila-Serrano NY, Rueda-Puente E (2006) Effects of foliar application of calcium nitrate on growth and physiological attributes of cowpea (Vigna unguiculata L. Walp.) grown under salt stress. Environ Exp Bot 58:188–196Google Scholar
  101. 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 132:146–153PubMedGoogle Scholar
  102. Neill SJ, Desikan R, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1242PubMedGoogle Scholar
  103. Nie L, Shah S, Burd GI, Dixon DG, Glick BR (2002) Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol Biochem 40:355–361Google Scholar
  104. Nishio T, Morita T (1991) Studies on the occurrence of blossom-end rot in tomato (9): the mineral elements concentrations in tomato fruits and plants in relation to the occurrence of blossom-end rot. Sci Rep Shiga Prefecture Jr Coll 40:41–46Google Scholar
  105. Normander B, Hendriksen NB, Nybroe O (1999) Green fluorescent protein-marked Pseudomonas fluorescens: localization, viability, and activity in the natural barley rhizosphere. Appl Environ Microbiol 65:4646–4651PubMedGoogle Scholar
  106. Ozkutlu F, Turan M, Korkmaz K, Huang YM (2009) Assessment of heavy metal accumulation in the soils and hazelnut (Corylus avellena L.) from Black sea coastal region of Turkey. Asian J Chem 21:4371–4388Google Scholar
  107. Palavan-Unsal N, Arisan D (2009) Nitric oxide signalling in plants. Bot Rev 75:203–229Google Scholar
  108. Pennanen T, Frostegard A, Fritz H (1996) Phospholipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Appl Environ Microbiol 62:420–428PubMedGoogle Scholar
  109. Penrose DM, Glick BR (2001) Levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in exudates and extracts of canola seeds treated with plant growth promoting bacteria. Can J Microbiol 47:368–372PubMedGoogle Scholar
  110. Podile AR, Kishore KG (2006) Plant growth-promoting rhizobacteria. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 195–230Google Scholar
  111. Qadir M, Ghafoor A, Murtaza G (2000) Amelioration strategies for saline soils: a review. Land Degrad Dev 11:501–521Google Scholar
  112. Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160PubMedGoogle Scholar
  113. Robinson B, Russell C, Hedley M, Clothier B (2001) Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agric Ecosyst Environ 87:315–321Google Scholar
  114. Romkens P, Bouwman L, Japenga J, Draaisma C (2002) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ Pollut 116:109–121PubMedGoogle Scholar
  115. Saleh S, Huang XD, Greenberg BM, Glick BR (2004) Phytoremediation of persistent organic contaminants in the environment. In: Singh A, Ward O (eds) Soil biology, vol 1, Applied bioremediation and phytoremediation. Springer, Berlin, pp 115–134Google Scholar
  116. Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biol Technol 13:468–474Google Scholar
  117. Sanchez PA (1976) Properties and managenent of soil in the tropics. Wiley, New YorkGoogle Scholar
  118. Sandaa RA, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251PubMedGoogle Scholar
  119. Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedGoogle Scholar
  120. Sessitsch A, Puschenreiter M (2008) Endophytes and rhizosphere bacteria of plants growing in heavy metal-containing soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer, Berlin, pp 317–332Google Scholar
  121. Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170PubMedGoogle Scholar
  122. Siciliano SD, Germida JJ (1997) Bacterial inoculants of forage grasses that enhance degradation of 2-chlorobenzoic acid in soil. Environ Toxicol Chem 16:1098–1104Google Scholar
  123. Siciliano SD, Germida JJ (1999) Enhanced phytoremediation of chlorobenzoates in rhizosphere soil. Soil Biol Biochem 31:299–305Google Scholar
  124. Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallicion decontamination from soil. Appl Microbiol Biotechnol 61:405–412PubMedGoogle Scholar
  125. Smolders E, Degryse F (2002) Fate and effect of zinc from tire debris in soil. Environ Sci Tech 36:3706–3710Google Scholar
  126. Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. Adv Bot Res 51:283–320Google Scholar
  127. Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796PubMedGoogle Scholar
  128. Sutherland RA, Day JP, Bussen JO (2003) Lead concentrations, isotope ratios and source apportionment in road deposited sediments, Honolulu, Oahu, Hawaii. Water Air Soil Pollut 142:165–186Google Scholar
  129. Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates., Sunderland, MA, 690pGoogle Scholar
  130. Umrania VV (2006) Bioremediation of toxic heavy metals using acidothermophilic autotrophes. Bioresour Technol 97:1237–1242PubMedGoogle Scholar
  131. USDA and NRSC (2000) Soil Quality Institute, Urban Technical Note No: 3. United States Department of Agriculture and National Resources Conservation ServiceGoogle Scholar
  132. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586Google Scholar
  133. Viklander M (1998) Particle size distribution and metal content in street sediments. J Environ Eng 124:761–766Google Scholar
  134. 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
  135. Vranova E, Inze D, van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236PubMedGoogle Scholar
  136. Wang Z, Huang B, Xu Q (2003) Effect of abscisic acid on drought response of Kentucky bluegrass. J Am Soc Hortic Sci 128:36–41Google Scholar
  137. Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598PubMedGoogle Scholar
  138. WHO (1997) Health and environment in sustainable development. WHO, GenevaGoogle Scholar
  139. Widada J, Damarjaya DI, Kabirun S (2007) The interactive effects of arbuscular mycorrhizal fungi and rhizobacteria on the growth and nutrients uptake of sorghum in acid soil. In: Velazquez E, Rodriguez-Barrueco C (eds) First ınternational meeting on microbial phosphate solubilization. Springer, Berlin, pp 173–177Google Scholar
  140. Woitke M, Junge H, Schnitzler WH (2004) Bacillus subtilis as growth promotor in hydroponically grown tomatoes under saline conditions. Acta Hortic 659:363–369Google Scholar
  141. Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135PubMedGoogle Scholar
  142. Yan-de J, Zhen-li, Xiao-e Y (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8:192–207Google Scholar
  143. Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114Google Scholar
  144. Yee DC, Maynard JA, Wood TK (1998) Rhizoremediation of trichloroethylene by a recombinant, root-colonizing Pseudomonas fluorescens strain expressing toluene ortho-monooxygenase constitutively. Appl Environ Microbiol 64:112–118PubMedGoogle Scholar
  145. Yildirim E, Taylor AG, Spittler TD (2006) Ameliorative effects of biological treatments on growth of squash plants under salt stress. Sci Hortic 111:1–6Google Scholar
  146. Yildirim E, Turan M, Donmez MF (2008a) Mitigation of salt stress in radish (Raphanus sativus l.) by plant growth promoting rhizobacteria. Rouman Biotech Let 13:3933–3943Google Scholar
  147. Yildirim E, Donmez MF, Turan M (2008b) Use of bioinoculants in ameliorative effects on radish plants under salinity stress. J Plant Nutr 31:2059–2074Google Scholar
  148. Zahir AZ, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168Google Scholar
  149. 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
  150. Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress. Crit Rev Plant Sci 16:253–277Google Scholar
  151. 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 2012

Authors and Affiliations

  1. 1.Department of Soil ScienceAtaturk UniversityErzurumTurkey
  2. 2.Department of HorticultureSelcuk UniversityKonyaTurkey
  3. 3.Department of Genetics and BioengineeringYeditepe UniversityKayisdagiTurkey

Personalised recommendations