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Plant Growth-Promoting Rhizobacteria for Abiotic Stress Alleviation in Crops

  • Sangeeta Paul
  • Ajinath S. Dukare
  • Bandeppa
  • B. S. Manjunatha
  • K. AnnapurnaEmail author
Chapter
Part of the Microorganisms for Sustainability book series (MICRO, volume 4)

Abstract

Environmental stresses pose a major constraint to agricultural productivity. Studies have indicated an immense potential of plant growth-promoting rhizobacteria (PGPRs) in the mitigation of different abiotic stresses in crops such as temperature, salinity, drought, heavy metal toxicity, etc. Improved plant growth and yield; and enhanced tolerance to various abiotic stresses due to inoculation with PGPRs have been noted in different plants. PGPRs mitigate environmental stress in plants through an array of mechanisms which include phytohormone production, induced systemic tolerance through modulation of physiological responses, osmotic adjustments through production of osmolytes, ACC deaminase activity, exopolysaccharide production, improvement in soil physicochemical properties, production of volatile organic carbon compounds, and induction of stress-responsive genes. Screening, selection, and use of abiotic stress-tolerant PGPRs as bioinoculants are a promising strategies for enhancing crop productivity under stressed environments.

Keywords

Plant growth-promoting rhizobacteria Abiotic stress alleviation Induced systemic tolerance Hormonal homeostasis ACC deaminase activity 

References

  1. Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886CrossRefPubMedGoogle Scholar
  2. Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by exopolysaccharide producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398CrossRefPubMedPubMedCentralGoogle Scholar
  3. Albacete A, Ghanem ME, Martıńez-Andujar C, Acosta M, Sanchez-Bravo J, Martinez V, Lutts S, Dodd IC, Perez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131Google Scholar
  4. Ali SZ, Sandhya V, Grover M, Rao LV, Kishore VN, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils 46:45–55CrossRefGoogle Scholar
  5. Al-Karaki GN (2001) Salt stress response of salt-sensitive and tolerant durum wheat cultivars inoculated with mycorrhizal fungi. Acta Agronomica Hung 49:25–34Google Scholar
  6. Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl Environ Microbiol 64:3740–3747PubMedPubMedCentralGoogle Scholar
  7. Ansary MH, Rahmani HA, Ardakani MR, Paknejad F, Habibi D, Mafakheri S (2012) Effect of Pseudomonas fluorescens on proline and phytohormonal status of maize (Zea mays L.) under water deficit stress. Ann Biol Res 3:1054–1062Google Scholar
  8. Arkipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315CrossRefGoogle Scholar
  9. Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.) Pedosphere 18:611–620Google Scholar
  10. Asch F, Padham JL (2005) Root associated bacteria suppress symptoms of iron toxicity in lowland rice. In: Tielkes E, Hulsebusch Hauser I, Deininger A, Becker K (eds) The global food & product chain – dynamics, innovations, conflicts, strategies. MDD GmbH, Stuttgart, p 276Google Scholar
  11. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376CrossRefGoogle Scholar
  12. Awad NM, Turky AS, Abdelhamid MT, Attia M (2012) Ameliorate of environmental salt stress on the growth of Zea mays L. plants by exopolysaccharides producing bacteria. J Appl Sci Res 8:2033–2044Google Scholar
  13. Bandeppa PS, Paul S, Kandpal BK (2015) Evaluation of osmotolerant rhizobacteria for alleviation of water deficit stress in mustard. Green Farm 6:590–593Google Scholar
  14. Bano A, Fatima M (2009) Salt tolerance in Zea mays L. following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413CrossRefGoogle Scholar
  15. Bano Q, Ilyas N, Bano A, Zafar N, Akram A, Hassan F (2013) Effect of Azospirillum inoculation on maize (Zea mays L.) under drought stress. Pak J Bot 45:13–20Google Scholar
  16. Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14CrossRefGoogle Scholar
  17. Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmas strain PsJN. Appl Environ Microbiol 72:7246–7252Google Scholar
  18. Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting Rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1228CrossRefGoogle Scholar
  19. Bashan Y, Holguin G, de-bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural and environmental advances (1997-2003). Can J Microbiol 50:521–577Google Scholar
  20. 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) 73:99–106CrossRefGoogle Scholar
  21. Bensalim S, Nowak J, Asiedu SK (1998) A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am J Potato Res 75:145–152Google Scholar
  22. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107CrossRefPubMedGoogle Scholar
  23. Blaha D, Prigent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470CrossRefPubMedGoogle Scholar
  24. Boyer JS (1982) Plant productivity and environment. Science 218:443–448Google Scholar
  25. Bresson J, Varoquaux F, Bontpart T, Touraine B, Vile D (2013) The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:1112–1123Google Scholar
  26. Breusegem FV, Vranová E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414Google Scholar
  27. Busk PK, Pagés M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435Google Scholar
  28. Carrillo-Castaneda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2003) Plant growth-promoting bacteria promote copper and iron translocation from root to shoot in alfalfa seedlings. J Plant Nutr 26:1801–1814CrossRefGoogle Scholar
  29. Carrillo-Castaneda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2005) Modulation of uptake and translocation of iron and copper from root to shoot in common bean by siderophore-producing microorganisms. J Plant Nutr 28:1853–1865CrossRefGoogle Scholar
  30. Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350Google Scholar
  31. Cassán F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19Google Scholar
  32. Chakraborty U, Chakraborty BN, Chakraborty AP, Dey PL (2013) Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J Microbiol Biotechnol 29:789–803CrossRefPubMedGoogle Scholar
  33. Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20Google Scholar
  34. Chen M, Wei H, Cao J, Liu R, Wang Y, Zheng C (2007) Expression of Bacillus subtilis proAB genes and reduction of feedback inhibition of proline synthesis increases proline production and confers osmotolerance in transgenic Arabdopsis. J Biochem Mol Biol 40:396–403PubMedGoogle Scholar
  35. 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 53:912–918CrossRefPubMedGoogle Scholar
  36. Cho K, Toler H, Lee J, Ownley BH, Stutz JC, Moore JL, Augé RM (2006) Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J Plant Physiol 163:517–528CrossRefPubMedGoogle Scholar
  37. Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R, 3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:1067–1075CrossRefPubMedGoogle Scholar
  38. Cho JA, Lee AH, Platzer B, Cross BC, Gardner BM, De Luca H (2013) The unfolded protein response element IRE1 alpha senses bacterial proteins invading the ER to activate RIG-I and innate immune signaling. Cell Host Microbe 13:558–569CrossRefPubMedPubMedCentralGoogle Scholar
  39. Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103CrossRefGoogle Scholar
  40. Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462Google Scholar
  41. Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Can J Bot 82:273–281CrossRefGoogle Scholar
  42. Del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81Google Scholar
  43. Del-Amor FM, Cuadra-Crespo P (2012) Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct Plant Biol 39:82–90CrossRefGoogle Scholar
  44. Dimkpa C, Weinand T, Asch F (2009a) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694CrossRefPubMedGoogle Scholar
  45. Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E (2009b) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162CrossRefGoogle Scholar
  46. Dodd IC, Belimov AA, Sobeih WY, Safronova VI, Grierson D, Davies WJ (2004) Will modifying plant ethylene status improve plant productivity in water limited environments? 4th International Crop Sciences Congress. Brisbane, Australia, 26 September–1 October 2004Google Scholar
  47. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864CrossRefGoogle Scholar
  48. Egamberdieva D, Kucharova Z (2009) Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571CrossRefGoogle Scholar
  49. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189CrossRefGoogle Scholar
  50. Egamberdiyeva D, Hoflich G (2003) Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biol Biochem 35:973–978Google Scholar
  51. Enebak SA, Wei G, Kloepper JW (1998) Effects of plant growth-promoting rhizobacteria on loblolly and slash pine seedlings. For Sci 44:139–144Google Scholar
  52. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:85–212CrossRefGoogle Scholar
  53. Geddie JL, Sutherland IW (1993) Uptake of metals by bacterial polysaccharides. J Appl Bacteriol 74:467–472CrossRefGoogle Scholar
  54. Ghosh S, Penterman JN, Little RD, Chavez R, Glick BR (2003) Three newly isolated plant growth promoting bacilli facilitate the seedling growth of canola seedlings. Plant Physiol Biochem 41:277–281Google Scholar
  55. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109−117Google Scholar
  56. Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242Google Scholar
  57. Gontia-Mishra I, Sasidharan S, Tiwari S (2014) Recent developments in use of 1-aminocyclopropane-1-carboxylate (ACC) deaminase for conferring tolerance to biotic and abiotic stress. Biotechnol Lett 36:889–898CrossRefPubMedGoogle Scholar
  58. Govindasamy V, Senthilkumar M, Gaikwad K, Annapurna K (2008) Isolation and characterization of ACC deaminase gene from two plant growth promoting rhizobacteria. Curr Microbiol 57:312–317CrossRefPubMedGoogle Scholar
  59. Govindasamy V, Senthilkumar M, Mageshwaran V, Annapurna K (2009) Detection and characterization of ACC deaminase in plant growth promoting rhizobacteria. J Plant Biochem Biotechnol 18:71–76CrossRefGoogle Scholar
  60. Govindasamy V, Senthilkumar M, Bose P, Vithalkumar L, Ramadoss D, Annapurna K (2011) ACC deaminase containing PGPR for potential exploitation in agriculture. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin/Heidelberg, pp 183–208CrossRefGoogle Scholar
  61. Govindasamy V, Senthilkumar M, Annapurna K (2015) Effect of mustard rhizobacteria on wheat growth promotion under cadmium stress: characterization of acdS gene coding ACC deaminase. Ann Microbiol 65:1679–1687CrossRefGoogle Scholar
  62. Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase containing plant growth-promoting bacteria. Plant Physiol Biochem 39:11–17Google Scholar
  63. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW (2013) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32:245–258CrossRefGoogle Scholar
  64. Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93CrossRefGoogle Scholar
  65. Hamaoui B, Abbadi JM, Burdman S, Rashid A, Sarig S, Okon Y (2001) Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomie 21:553–560CrossRefGoogle Scholar
  66. Hamdia ABE, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasiliense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44:165–174CrossRefGoogle Scholar
  67. Han HS, Lee KD (2005) Physiological responses of soybean-inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agric Biol Sci 1:216–221Google Scholar
  68. Hare PD, Cress WA, Staden VJ (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  69. Hernandez M, Chailloux M (2004) Las micorrizas arbusculares y las bacterias rizosfericas como alternativa a la nutricion mineral del tomate. Cultivos Tropicales 25:5–16Google Scholar
  70. Huang XD, El-Alawi YS, 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. Iqbal N, Ashraf Y, Ashraf M (2011) Modulation of endogenous levels of some key organic metabolites by exogenous application of glycine betaine in drought stressed plants of sunflower (Helianthus annuus L.). Plant Growth Regul 63:7–12Google Scholar
  72. Jacobson CB, Pasternak JJ, Glick RB (1994) Partial purification and characterization of 1-aminocyclopropane-l- carboxylate deaminase from the plant growth promoting rhizobacterium, Pseudomonas putida GR12-2. Can J Microbiol 40:1019–1025Google Scholar
  73. Jha Y, Subramanian RB, Patel S (2010) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802Google Scholar
  74. Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832CrossRefPubMedGoogle Scholar
  75. Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal polluted soil. Chemosphere 72:157–164CrossRefPubMedGoogle Scholar
  76. Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014a) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682Google Scholar
  77. Kang SM, Radhakrishnan R, Khan AL, Kim MJ, Park JM, Kim BR, Shin DH, Lee IJ (2014b) Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84:115–124Google Scholar
  78. Kloepper JW, Gutierrez-Estrada A, Mclnroy JA (2007) Photoperiod regulates elicitation of growth promotion but not induced resistance by plant growth-promoting rhizobacteria. Can J Microbiol 53:159–167CrossRefPubMedGoogle Scholar
  79. Kohler J, Hernandez JA, Caravaca F, Roldan A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water stressed plants. Funct Plant Biol 35:141–151CrossRefGoogle Scholar
  80. Kohler J, Hernandez JA, Caravaca F, Roldàn 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 65:245–252CrossRefGoogle Scholar
  81. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608Google Scholar
  82. Lee YH, HS O, Cheon CI, Hwang IT, Kim YJ, Chun JY (2001) Structure and expression of the Arabidopsis thaliana homeobox gene Athb-12. Biochem Biophys Res Commun 284:133–141Google Scholar
  83. Liddycoat SM, Greenberg BM, Wolyn DJ (2009) The effect of plant growth-promoting rhizobacteria on asparagus seedlings and germinating seeds subjected to water stress under greenhouse conditions. Can J Microbiol 55:388–394Google Scholar
  84. Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201–208Google Scholar
  85. Liu J, Mehdi S, Topping J, Friml J, Lindsey K (2013) Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development. Front Plant Sci 4:75PubMedPubMedCentralGoogle Scholar
  86. Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacterium reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69:220–228Google Scholar
  87. Maheshwari DK, Kumar S, Maheshwari NK, Patel D, Saraf M (2012) Nutrient availability and management in the rhizosphere by microorganisms. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin/Heidelberg, pp 301–325CrossRefGoogle Scholar
  88. Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 55:27–34CrossRefPubMedGoogle Scholar
  89. Marulanda A, Porcel R, Barea JM, Azcon R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought tolerant or drought sensitive Glomus species. Microb Ecol 54:543–552CrossRefPubMedGoogle Scholar
  90. Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530CrossRefGoogle Scholar
  91. Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefPubMedGoogle Scholar
  92. McLellan CA, Turbyville TJ, Kithsiri Wijeratne EM, Kerschen A, Vierling E, Queitsch C, Whitesell L, Leslie Gunatilaka AA (2007) A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol 145:174–182Google Scholar
  93. Mishra PK, Bisht SC, Bisht JK, Bhatt JC (2012) Cold-tolerant PGPRs as bioinoculants for stress management. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin/Heidelberg, pp 95–118CrossRefGoogle Scholar
  94. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefPubMedGoogle Scholar
  95. Munchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in rhizobia. J Bacteriol 181:83–90Google Scholar
  96. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  97. Nabti E, Sahnoune M, Adjrad S, Van Dommelen A, Ghoul M, Schmid M, Hartmann A (2007) A halophilic and osmotolerant Azospirillum brasilense strain from Algerian soil restores wheat growth under saline conditions. Eng Life Sci 7:354–360CrossRefGoogle Scholar
  98. 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 53:1141–1149CrossRefPubMedGoogle Scholar
  99. Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant- microbe interactions using a rhizosphere metabolomics – driven approach and its applications in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153Google Scholar
  100. Nayer M, Heidari R (2008) Drought-induced accumulation of soluble sugars and proline in two maize varieties. World App Sci J 3:448–453Google Scholar
  101. Naz I, Bano A, Hassan TU (2009) Isolation of phytohormones producing plant growth promoting rhizobacteria from weeds growing in Khewra salt range, Pakistan and their implication in providing salt tolerance to Glycine max L. African J Biotech 8:5762–5766CrossRefGoogle Scholar
  102. Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:182–186CrossRefGoogle Scholar
  103. Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Guimaraes CT, Schaffert RE, Sa NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787Google Scholar
  104. Omar MNA, Osman MEH, Kasim WA, Abd El-Daim IA (2009) Improvement of salt tolerance mechanisms of barley cultivated under salt stress using Azospirillum brasilense. In: Ashraf M, Ozturk M, Athar HR (eds) Salinity and water stress improving crop efficiency, Tasks for vegetation sciences, vol 44. Springer, Dordrecht, pp 133–147Google Scholar
  105. Patakas A, Noitsakis B (2001) Leaf age effects on solute accumulation in water stressed grapevines. J Plant Physiol 158:63–69Google Scholar
  106. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3- acetic acid. Can J Microbiol 42:207–220CrossRefPubMedGoogle Scholar
  107. Paul D, Nair S (2008) Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48:378–384Google Scholar
  108. Pereyra MA, García P, Colabelli MN, Barassi CA, Creus CM (2012) A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Appl Soil Ecol 53:94–97CrossRefGoogle Scholar
  109. Pishchik VN, Provorov NA, Vorobyov NI, Chizevskaya EP, Safronova VI, Tuev AN, Kozhemyakov AP (2009) Interactions between plants and associated bacteria in soils contaminated with heavy metals. Microbiology 78:785–793CrossRefGoogle Scholar
  110. Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764CrossRefPubMedGoogle Scholar
  111. Price A, Lucas PW, Lea PJ (1990) Age dependent damage and glutathione metabolism in ozone fumigated barley: a leaf section approach. J Exp Bot 41:1309–1317Google Scholar
  112. Rejeb I, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3:458–475CrossRefPubMedPubMedCentralGoogle Scholar
  113. Rincon A, Valladares F, Gimeno TE, Pueyo JJ (2008) Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiol 28:1693–1701CrossRefPubMedGoogle Scholar
  114. Roberson EB, Firestone M (1992) Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl Environ Microbiol 58:1284–1291PubMedPubMedCentralGoogle Scholar
  115. Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59Google Scholar
  116. Rokhzadi A, Toashih V (2011) Nutrient uptake and yield of chickpea (Cicer arietinum L.) inoculated with plant growth-promoting rhizobacteria. Aus J Crop Sci 5:44–48Google Scholar
  117. Ruiz-Sanchez M, Armada E, Munoz Y, Garcia de Salamone IE, Aroca R, Ruiz-Lozano JM, Azcon R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well watered and drought conditions. J Plant Physiol 168:1031–1037CrossRefPubMedGoogle Scholar
  118. Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88CrossRefPubMedGoogle Scholar
  119. Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26Google Scholar
  120. Sandhya V, Ali SZ, Grover M, Gopal R, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30CrossRefGoogle Scholar
  121. Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10:393CrossRefPubMedPubMedCentralGoogle Scholar
  122. Selvakumar G, Panneerselvam P, Ganeshamurthy AN (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, New York, pp 205–224CrossRefGoogle Scholar
  123. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292Google Scholar
  124. Sessitsch A, Reiter B, Berg G (2005) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249CrossRefGoogle Scholar
  125. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.) Lett Appl Microbiol 42:155–159CrossRefPubMedGoogle Scholar
  126. Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155Google Scholar
  127. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151CrossRefPubMedGoogle Scholar
  128. 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 156:1164–1170Google Scholar
  129. Siddikee MA, Chauhan PS, Anandham R, Han GH, Sa T (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584Google Scholar
  130. Siddikee MA, Glick BR, Chauhan PS, Wj Y, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434Google Scholar
  131. Singh R, Soni SK, Patel RP, Kalra A (2013) Technology for improving essential oil yield of Ocimum basilicum L. (sweet basil) by application of bioinoculant colonized seeds under organic field conditions. Ind Crop Prod 45:335–342Google Scholar
  132. Srivastava S, Yadav A, Seem K, Mishra S, Choudhary V, Nautiyal CS (2008) Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr Microbiol 56:453–457Google Scholar
  133. Stajner D, Kevreaan S, Gasaić O, Mimica-Dudić N, Zongli H (1997) Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol Plant 39:441–445Google Scholar
  134. Strzelczyk E, Kampert M, Pachlewski R (1994) The influence of pH and temperature on ethylene production by mycorrhizal fungi of pine. Mycorrhiza 4:193–196CrossRefGoogle Scholar
  135. Swaine EK, Swaine MD, Killham K (2007) Effects of drought on isolates of Bradyrhizobium elkanii cultured from Albizia adianthifolia seedlings on different provenances. Agrofor Syst 69:135–145CrossRefGoogle Scholar
  136. Terré S, Asch F, Padham J, Sikora RA, Becker M (2007) Influence of root zone bacteria on root iron plaque formation in rice subjected to iron toxicity. In: Tielkes E (ed) Utilisation of diversity in land use systems: sustainable and organic approaches to meet human needs. Tropentag, Witzenhausen, p 446Google Scholar
  137. Timmusk S, Nevo E (2011) Plant root associated biofilms. In: Maheshwari DK (ed) Bacteria in agrobiology (vol 3) plant nutrient management. Springer, Berlin, pp 285–300CrossRefGoogle Scholar
  138. Timmusk S, Wagner EG (1999) The plant-growth promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant-Microbe Interact 12:951–959Google Scholar
  139. Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. Eur J Soil Sci 33:141–163Google Scholar
  140. Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC-transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340CrossRefPubMedGoogle Scholar
  141. Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14Google Scholar
  142. Verbon EH, Liberman LM (2016) Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci 21:218–229CrossRefPubMedPubMedCentralGoogle Scholar
  143. Vinagre F, Vargas C, Schwarcz K, Cavalcante J, Nogueira EM, Baldani JI, Ferreira PC, Hemerly AS (2006) SHR5: a novel plant receptor kinase involved in plant-N2-fixing endophytic bacteria association. J Exp Bot 57:559–569Google Scholar
  144. Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 165:60–70Google Scholar
  145. Wang CY (1987) Changes of polyamines and ethylene in cucumber seedlings in response to chilling stress. Plant Physiol 69:253–257CrossRefGoogle Scholar
  146. Wang WX, Vinocur B, Shoseyov O, Altman A (2001) Biotechnology of plant osmotic stress tolerance physiological and molecular considerations. Acta Hortic 560:285–292Google Scholar
  147. Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth promoting rhizobacterium strains. PLoS One 7:e52565Google Scholar
  148. Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340Google Scholar
  149. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264CrossRefPubMedPubMedCentralGoogle Scholar
  150. Yao L, Wu Z, Zheng Y, Kaleem I, Li C (2010) Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur J Soil Biol 46:49–54CrossRefGoogle Scholar
  151. Yasmin H, Bano A (2011) Isolation and characterization of phosphate solubilizing bacteria from rhizosphere soil of weeds of Khewra salt range and Attock. Pak J Bot 43:1663–1668Google Scholar
  152. Yazdani M, Bahmanyar MA, Pirdashti H, Esmaili MA (2009) Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Acd Sci Eng Technol 49:90–92Google Scholar
  153. Yildirim E, Taylor AG (2005) Effect of biological treatments on growth of bean plans under salt stress. Ann Rep Bean Improv Coop 48:176–177Google Scholar
  154. Yildirim E, Turan M, Donmez MF (2008) Mitigation of salt stress in radish (Raphanus sativus L.) by plant growth promoting rhizobacteria. Roumanian Biotechnol Lett 13:3933–3943Google Scholar
  155. Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi- Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102Google Scholar
  156. Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agri Res 56:715–721CrossRefGoogle Scholar
  157. Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963Google Scholar
  158. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851Google Scholar
  159. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant-Microbe Interact 21:737–744Google Scholar
  160. Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant-Microbe Interact 23:1097–1104Google Scholar
  161. Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, Sheng XF (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62CrossRefPubMedGoogle Scholar
  162. Zuccarini P, Okurowska P (2008) Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J Plant Nutr 31:497–513Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Sangeeta Paul
    • 1
  • Ajinath S. Dukare
    • 2
  • Bandeppa
    • 3
  • B. S. Manjunatha
    • 1
  • K. Annapurna
    • 1
    Email author
  1. 1.Division of MicrobiologyICAR-Indian Agricultural Research InstituteNew DelhiIndia
  2. 2.Division of Horticulture Crop ProcessingICAR-Central Institute of Post-Harvest Engineering & TechnologyAboharIndia
  3. 3.Division of Soil ScienceICAR-Indian Institute of Rice ResearchHyderabadIndia

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