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Rhizobacteria as Bioprotectants Against Stress Conditions

  • F. Pereira
Chapter
Part of the Microorganisms for Sustainability book series (MICRO, volume 12)

Abstract

The area around the plant which is under the influence of plant roots, known as the rhizosphere, is an attractive habitat for soil microorganisms. However, although a variety of root-colonizing bacteria exist, the beneficial bacteria also called plant growth-promoting bacteria (PGPR) or rhizobacteria essentially serve as bioprotectants against stress conditions. Environmental abiotic stresses such as drought, salinity, and metal contamination, as well as biotic stresses from opportunistic pathogens, present a major challenge as it reduces the potential yields of food production. Rhizobacteria are of immense interest because they compete with indigenous bacteria and increase plant resistance against stress conditions. These bacteria have a number of traits that contribute to root colonization such as the presence of specific cell surface components, pili, fimbriae, chemotaxis toward plant exudates, ability to use specific components of plant exudates, protein secretion property, ability to form biofilms, and quorum sensing. The production of biologically active metabolites and the regulation of ACC deaminase are some of the principal mechanisms by which rhizobacteria modify the rhizosphere environment thereby enhancing plant growth. This article seeks to give an overview of mechanisms in rhizobacteria proposed to enhance stress tolerance conditions.

Keywords

Rhizobacteria Abiotic stress Stress tolerance Plant growth 

Notes

Acknowledgments

The author is grateful to the Principal of P.E.S’s RSN College for his support.

References

  1. Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66(8):3393–3398PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ali SKZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils 46:45–55CrossRefGoogle Scholar
  3. Ali SKZ, Sandhya V, Grover M, Rao LV, Venkateswarlu B (2011) Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J Plant Interact 6:239–246CrossRefGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  5. Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315.  https://doi.org/10.1007/s11104-007-9233-5CrossRefGoogle Scholar
  6. Asch F, Padham JL (2005) Root associated bacteria suppress symptoms of iron toxicity in lowland rice. In: Tielkes E, Hülsebusch C, Häuser I, Deininger A, Becker K (eds) The global food & product chain – dynamics, innovations, conflicts, strategies. MDD GmbH, Stuttgart, p 276Google Scholar
  7. Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Rev Plant Sci 23:157–174CrossRefGoogle Scholar
  8. Aslantas R, Cakmakci R, Sahin F (2007) Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Sci Hortic 111:371–377CrossRefGoogle Scholar
  9. Azar F, Mozafari V, Dahaji PA, Hamidpour M (2016) Biochemical, physiological and antioxidant enzymatic activity responses of pistachio seedlings treated with plant growth promoting rhizobacteria and Zn to salinity stress. Acta Physiol Plant 38:21CrossRefGoogle Scholar
  10. Bais HP, Loyola Vargas VM, Flores HE, Vivanco JM (2001) Root specific metabolism: the biology and biochemistry of underground organs. In Vitro Cell Dev Biol Plant 37:730–741CrossRefGoogle Scholar
  11. Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of sweet basil (Ocimum basilicum L.). Plant Physiol Biochem 40:983–995CrossRefGoogle Scholar
  12. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trend Plant Sci 9:26–32CrossRefGoogle Scholar
  13. Banerjee S, Palit R, Sengupta C, Standing D (2010) Stress induced phosphate solubilization by Arthrobacter sp. and Bacillus sp. isolated from tomato rhizosphere. Aust J Crop Sci 4(6):378–383Google Scholar
  14. Barber DA, Martin JK (1976) The release of organic substances by cereal roots in soil. New Phytol 76:69–80CrossRefGoogle Scholar
  15. Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778CrossRefGoogle Scholar
  16. Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A (2017) Plant growth promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 161:502–514.  https://doi.org/10.1111/ppl.12614CrossRefGoogle Scholar
  17. Bell TH, Callender KL, Whyte LG, Greer CW (2013) Microbial competition in polar soils: a review of an understudied but potentially important control on productivity. Biology 2(2):533–554.  https://doi.org/10.3390/biology2020533CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 75:145–152CrossRefGoogle Scholar
  19. Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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(11):3097–3107.  https://doi.org/10.1093/jxb/erp140CrossRefPubMedGoogle Scholar
  21. Bianco C, Defez R (2011) Soil bacteria support and protect plants against abiotic stresses. In: Shanker A (ed) Abiotic stress in plants. IntechOpen, pp 143–170.  https://doi.org/10.5772/23310Google Scholar
  22. Bisseling T, Dangl JL, Schulze-Lefert P (2009) Next-generation communication. Science 324:691.  https://doi.org/10.1126/science.1174404CrossRefPubMedGoogle Scholar
  23. Brigham LA, Michaels PJ, Flores HE (1999) Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon. Plant Physiol 119:417–428PubMedPubMedCentralCrossRefGoogle Scholar
  24. Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64(10):3663–3668PubMedPubMedCentralGoogle Scholar
  25. Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46(3):237–245.  https://doi.org/10.1139/w99-143CrossRefPubMedPubMedCentralGoogle Scholar
  26. Buscot F (2005) What are soils? In: Buscot F, Varma S (eds) Micro-organisms in soils: roles in genesis and functions. Springer, Heidelberg, pp 3–18CrossRefGoogle Scholar
  27. 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(7):912–918PubMedCrossRefGoogle Scholar
  28. Chun Juan W, Ya Hui G, Chao W, Hong Xia L, Dong Dong N, Yun Peng W, Jian Hua G (2012) Enhancement of tomato (Lycopersicon esculentum) tolerance to drought stress by plant-growth-promoting rhizobacterium (PGPR) Bacillus cereus AR156. J Agric Biotechnol 20:1097–1105Google Scholar
  29. Crowley DE (2006) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadía J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 169–198CrossRefGoogle Scholar
  30. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. In: Adu-Gyamfi JJ (ed) Food security in nutrient-stressed environments: exploiting plants’ genetic capabilities, Developments in Plant and Soil Sciences, vol 95. Springer, Dordrecht, pp 201–213.  https://doi.org/10.1007/978-94-017-1570-6_23CrossRefGoogle Scholar
  31. Dashti N, Zhang F, Hynes R, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil 200(2):205–213.  https://doi.org/10.1023/A:1004358100856CrossRefGoogle Scholar
  32. Daur I, Saad MM, Eida AA, Ahmad S, Shah ZH, Ihsan MZ, Muhammad Y, Sohrab SS, Hirt H (2018) Boosting Alfalfa (Medicago sativa L.) production with rhizobacteria from various plants in Saudi Arabia. Front Microbiol 9:477.  https://doi.org/10.3389/fmicb.2018.00477CrossRefPubMedPubMedCentralGoogle Scholar
  33. Dekkers LC, Phoelich CC, Lugtenberg BJJ (1999) Bacterial traits and genes involved in rhizosphere colonization in microbial biosystems: new frontiers proceedings of the 8th international symposium on microbial ecology. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Atlantic Canada society for microbial ecology, Halifax, CanadaGoogle Scholar
  34. Del Gallo M, Fendrik I (1994) The rhizosphere and Azospirillum. In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, pp 57–75Google Scholar
  35. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40(1):74–84. ISSN: 0038-0717.  https://doi.org/10.1016/j.soilbio.2007.06.024CrossRefGoogle Scholar
  36. Dimkpa CO, Svatoš A, Merten D, Büchel G, Kothe E (2008a) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172PubMedCrossRefGoogle Scholar
  37. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008b) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74(1):19–25.  https://doi.org/10.1016/j.chemosphere.2008.09.079CrossRefPubMedGoogle Scholar
  38. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009a) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162CrossRefGoogle Scholar
  39. Dimkpa CO, Weinand T, Asch F (2009b) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694.  https://doi.org/10.1111/j.1365-3040.2009.02028.xCrossRefGoogle Scholar
  40. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149.  https://doi.org/10.1080/713610853CrossRefGoogle Scholar
  41. Doornbos RF, Van Loon LC, Peter AHM, Bakker A (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. Rev Sustain Dev 32:227–243CrossRefGoogle Scholar
  42. Estabrook EM, Yoder JI (1998) Plant–plant communications: rhizosphere signaling between parasitic angiosperms and their probes. Plant Physiol 116:1–7PubMedCentralCrossRefPubMedGoogle Scholar
  43. Fernàndez LA, Berenguer J (2000) Secretion and assembly of regular surface structures in Gram-negative bacteria. FEMS Microbiol Rev 24:21–44PubMedCrossRefGoogle Scholar
  44. Figueiredo MVB, Burity HA, Martinez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co- inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188CrossRefGoogle Scholar
  45. Flores HE, Vivanco JM, Loyola-Vargas VM (1999) “Radicle” biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226PubMedCrossRefGoogle Scholar
  46. Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152.  https://doi.org/10.1007/s00253-007-1077-7CrossRefPubMedGoogle Scholar
  47. Fukami J, Ollero FJ, Megías M, Hungria M (2017) Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Exp 7:153.  https://doi.org/10.1186/s13568-017-0453-7CrossRefGoogle Scholar
  48. García-Cristobal J, García-Villaraco A, Ramos B, Gutierrez-Mañero J, Lucas JA (2015) Priming of pathogenesis related-proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. J Plant Physiol 188:72–79.  https://doi.org/10.1016/j.jplph.2015.09.011. Epub 2015 Sep 28CrossRefPubMedGoogle Scholar
  49. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7PubMedCrossRefPubMedCentralGoogle Scholar
  50. Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London.  https://doi.org/10.1142/p130CrossRefGoogle Scholar
  51. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  52. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319CrossRefGoogle Scholar
  53. Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang W, Lin M, Yan Y (2015) 1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25:1119–1128CrossRefGoogle Scholar
  54. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471.  https://doi.org/10.1016/j.tim.2008.07.008CrossRefPubMedPubMedCentralGoogle Scholar
  55. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Reg 21:79–102CrossRefGoogle Scholar
  56. Heidari M, Golpayegani A (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Soc Agric Sci 11(1):57–61Google Scholar
  57. Hendry GA (2005) Oxygen free radical process and seed longevity. Seed Sci J 3:141–147CrossRefGoogle Scholar
  58. Huang S, Dai Q, Peng S, Chavez AQ, Miranda LL, Visperas RM, Vergara BS (1997) Influence of supplemental ultraviolet-B on indole acetic acid and calmodulin in the leaves of rice (Oryza sativa L). Plant Growth Regul 21:59–64CrossRefGoogle Scholar
  59. Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33(3):797–802CrossRefGoogle Scholar
  60. Joo GJ, Kim YM, Kim JT, Rhee IK, Kim JH, Lee IJ (2005) Gibberellins-producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J Microbiol 43:510–515PubMedGoogle Scholar
  61. Kang S, Khan AL, Waqas M, You Y, Kim J, Hamayun M, Lee I (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9(1):673–682.  https://doi.org/10.1080/17429145.2014.894587CrossRefGoogle Scholar
  62. Kasotia A, Varma A, Tuteja N, Choudhary DK (2016) Microbial-mediated amelioration of plants under abiotic stress: an emphasis on arid and semiarid climate. In: Plant-microbe interaction: an approach to sustainable agriculture, pp 155–163.  https://doi.org/10.1007/978-981-10-2854-0_7CrossRefGoogle Scholar
  63. Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438Google Scholar
  64. Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In: Proceedings of the 4th international conference on plant pathogenic bacteria, vol 2. Station de Pathologie Végétale et de Phytobactériologie. INRA, Angers, pp 879–882Google Scholar
  65. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320CrossRefGoogle Scholar
  66. Lal S, Dhingra GK, Sharma S, Pokhriyal P, Das R, Gupta A, Kuriyal S (2011) UV-B irradiance induced deleterious effects on the net primary productivity and counteracted by some plant growth regulators (PGRs), in Brassica campestris PT-303 (brown sarson). Int J Plant Anim Environ Sci 1:202–209Google Scholar
  67. Lombard N, Prestat E, van Elsas JD, Simonet P (2011) Soil-specific limitations for access and analysis of soil microbial communities by metagenomics. FEMS Microbiol Ecol 78(1):31–49.  https://doi.org/10.1111/j.1574-6941.2011.01140.xCrossRefPubMedGoogle Scholar
  68. Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Inoculation of Brassica oxyrrhina with plant growth promoting bacteria for the improvement of heavy metal phytoremediation under drought conditions. J Hazard Mat 320:36–44CrossRefGoogle Scholar
  69. Mahmood S, Daur I, Al-Solaimani SG, Ahmad S, Madkour MH, Yasir M, Hirt H, Ali S, Ali Z (2016) Plant growth promoting rhizobacteria and silicon synergistically enhance salinity tolerance of mung bean. Front Plant Sci 7:876.  https://doi.org/10.3389/fpls.2016.00876CrossRefPubMedPubMedCentralGoogle Scholar
  70. Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43(4):491–500CrossRefGoogle Scholar
  71. Martin HV, Elliott MC (1984) Ontogenetic changes in the transport of indol-3yl-acetic acid into maize roots from the shoot and caryopsis. Plant Physiol 74:971–974PubMedPubMedCentralCrossRefGoogle Scholar
  72. Marulanda A, Barea J-M, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28(2):115–124CrossRefGoogle Scholar
  73. Marulanda A, Azcon R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–543CrossRefGoogle Scholar
  74. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449PubMedCrossRefGoogle Scholar
  75. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572.  https://doi.org/10.1016/j.plaphy.2004.05.009CrossRefGoogle Scholar
  76. McNear DH Jr (2013) The rhizosphere – roots, soil and everything in between. Nat Educ Knowl 4(3):1Google Scholar
  77. Merritt PM, Danhorn T, Fuqua C (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189:8005–8014PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nair A, Abraham TK, Jaya DS (2008) Studies on the changes in lipid peroxidation and antioxidants in drought stress induced in cowpea (Vigna unguiculata L.) varieties. J Environ Biol 29:689–691PubMedGoogle Scholar
  79. Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 5:653–658CrossRefGoogle Scholar
  80. Naznin HA, Kimura M, Miyazawa M, Hyakumachi M (2012) Analysis of volatile organic compounds emitted by plant growth promoting fungus Phoma sp. GS8- 3 for growth promotion effects on tobacco. Microbe Environ 28:42–49CrossRefGoogle Scholar
  81. Nehra V, Saharan BS, Choudhary M (2016) Evaluation of Brevibacillus brevis as a potential plant growth promoting rhizobacteria for cotton (Gossypium hirsutum) crop. Springer Plus 5:948.  https://doi.org/10.1186/s40064-016-2584-8CrossRefPubMedGoogle Scholar
  82. Newman EI (1985) The rhizosphere: carbon sources and microbial populations. In: Fitter AH (ed) Ecological interactions in soil. Blackwell Scientific Publications, Oxford, p 107Google Scholar
  83. Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río RE, Campos-García J, López-Bucio J (2011) Trans kingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci 108(17):7253–7258.  https://doi.org/10.1073/pnas.1006740108CrossRefPubMedGoogle Scholar
  84. Oves M, Khan MS, Zaidi A (2013) Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol 56:72–83CrossRefGoogle Scholar
  85. Paredes-Páliz K, Rodríguez-Vázquez R, Duarte B, Caviedes MA, Mateos-Naranjo E, Redondo-Gómez S, Caçador MI, Rodríguez-Llorente ID, Pajuelo E (2018) Investigating the mechanisms underlying phytoprotection by plant growth-promoting rhizobacteria in Spartina densiflora under metal stress. Plant Biol (Stuttg) 20(3):497–506.  https://doi.org/10.1111/plb.12693. Epub 2018 Mar 6CrossRefGoogle Scholar
  86. Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68(8):3795–3801.  https://doi.org/10.1128/AEM.68.8.3795-3801.2002CrossRefPubMedPubMedCentralGoogle Scholar
  87. 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(5):378–84PubMedCrossRefGoogle Scholar
  88. Paul D, Dineshkumar N, Nair S (2006) Proteomics of a plant growth-promoting rhizobacterium, Pseudomonas fluorescens MSP-393, subjected to salt shock. World J Microbiol Biotechnol 22(4):369–374.  https://doi.org/10.1007/s11274-005-9043-yCrossRefGoogle Scholar
  89. Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254(6):2201–2213.  https://doi.org/10.1007/s00709-017-1109-9. Epub 2017 Apr 12CrossRefGoogle Scholar
  90. Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75(5):1143–1150.  https://doi.org/10.1007/s00253-007-0909-9CrossRefPubMedGoogle Scholar
  91. Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environ 26(2):189–199CrossRefGoogle Scholar
  92. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980PubMedCrossRefGoogle Scholar
  93. Rahdari P, Hosseini SM, Tavakoli S (2012) The studying effect of drought stress on germination, proline, sugar, lipid, protein and chlorophyll content in purslane (Portulaca oleracea L.) leaves. J Med Plants Res 6(9):1539–1547.  https://doi.org/10.5897/JMPRCrossRefGoogle Scholar
  94. Rajendhran J, Gunasekaran P (2008) Strategies for accessing soil metagenome for desired applications. Biotechnol Adv 26(6):576–590PubMedCrossRefGoogle Scholar
  95. Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20PubMedCrossRefGoogle Scholar
  96. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, PierottiCei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331PubMedCrossRefGoogle Scholar
  97. Rovira AD (1969) Plant root exudates. Bot Rev 35(1):35–57CrossRefGoogle Scholar
  98. Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285.  https://doi.org/10.1007/s11104-004-0301-9CrossRefGoogle Scholar
  99. Sarkar J, Chakraborty B, Chakraborty U (2018a) Plant growth promoting rhizobacteria protect wheat plants against temperature stress through antioxidant signalling and reducing chloroplast and membrane injury. J Plant Growth Regul 1–17.  https://doi.org/10.1007/s00344-018-9789-8CrossRefGoogle Scholar
  100. Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S, Mondal MH, Maiti TK (2018b) A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32CrossRefGoogle Scholar
  101. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394CrossRefGoogle Scholar
  102. Schuhegger RM, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918PubMedCrossRefGoogle Scholar
  103. 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, Berlin, pp 205–224CrossRefGoogle Scholar
  104. Sgherri CLM, Maffei M, Navari-Izzo F (2000) Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. J Plant Physiol 157:273–279CrossRefGoogle Scholar
  105. Shah DA, Sen S, Shalini A, Ghosh D, Grover M, Mohapatra S (2017) An auxin secreting Pseudomonas putida rhizobacterial strain that negatively impacts water-stress tolerance in Arabidopsis thaliana. Rhizosphere 3(1):16–19CrossRefGoogle Scholar
  106. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158(3):243–248PubMedCrossRefGoogle Scholar
  107. Sheikh HH, Hossain K, Halimi MS (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int 2016: 6284547, 10 p.  https://doi.org/10.1155/2016/6284547CrossRefGoogle Scholar
  108. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125(1):27–58CrossRefGoogle Scholar
  109. Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630CrossRefGoogle Scholar
  110. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol 124:1007–1018PubMedPubMedCentralCrossRefGoogle Scholar
  111. Stringlis IA, Yu K, Feussner K, Jonge R, Bentum SV, Verk MCV, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci. 201722335.  https://doi.org/10.1073/pnas.1722335115CrossRefGoogle Scholar
  112. Su F, Jacquard C, Villaume S, Michel J, Rabenoelina F, Christophe C, Barka EA, Dhondt-Cordelier S, Vaillant-Gaveau N (2015) Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci 6:810.  https://doi.org/10.3389/fpls.2015.00810CrossRefPubMedPubMedCentralGoogle Scholar
  113. Takshak S, Agrawal SB (2014a) Effect of ultraviolet-B radiation on biomass production, lipid peroxidation, reactive oxygen species, and antioxidants in Withania somnifera. Biol Plant 58:328–334CrossRefGoogle Scholar
  114. Takshak S, Agrawal SB (2014b) Secondary metabolites and phenylpropanoid pathway enzymes as influenced under supplemental ultraviolet-B radiation in Withania somnifera Dunal, an indigenous medicinal plant. J Photochem Photobiol B 140:332–343PubMedCrossRefGoogle Scholar
  115. Thomsen IK, Schjønning P, Jensen B, Kristensen K, Christensen BT (1999) Turnover of organic matter in differently textured soils: II. Microbial activity as influenced by soil water regimes. Geoderma 89(3–4):199–218CrossRefGoogle Scholar
  116. Timmusk S, Wagner EGH (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 12:951–959PubMedCrossRefGoogle Scholar
  117. Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171.  https://doi.org/10.1128/AEM.68.5.2161-2171.2002CrossRefPubMedPubMedCentralGoogle Scholar
  118. Ullah U, Ashraf M, Sher MS, Siddiqui AR, Piracha MA, Muhammad S (2016) Growth behavior of tomato (Solanum lycopersicum L.) under drought stress in the presence of silicon and plant growth promoting rhizobacteria. Soil Environ 35(1):65–75Google Scholar
  119. Upadhyay SK, Singh JS, Singh DP (2011) Exopolysaccharide-producing plant growth- promoting rhizobacteria under salinity condition. Pedosphere 21(2):214–222CrossRefGoogle Scholar
  120. Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2010) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6(1):1–14.  https://doi.org/10.1080/17429145.2010.535178CrossRefGoogle Scholar
  121. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759CrossRefGoogle Scholar
  122. Vurukonda SSKP, Vardharajula S, Shrivastava M, Ali SKZ (2016a) Multifunctional Pseudomonas putida strain FBKV2 from arid rhizosphere soil and its growth promotional effects on maize under drought stress. Rhizosphere 1:4–13CrossRefGoogle Scholar
  123. Vurukonda SSKP, Vardharajula S, Shrivastava M, Ali SKZ (2016b) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24PubMedPubMedCentralCrossRefGoogle Scholar
  124. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1):44–51.  https://doi.org/10.1104/pp.102.019661CrossRefPubMedPubMedCentralGoogle Scholar
  125. Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):s131–s151.  https://doi.org/10.1105/tpc.001768CrossRefPubMedPubMedCentralGoogle Scholar
  126. Wang Q, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-aminocyclopropane-1- carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct Plant Biol 43:161–172.  https://doi.org/10.1071/FP15200CrossRefGoogle Scholar
  127. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4PubMedPubMedCentralCrossRefGoogle Scholar
  128. Yang A, Saleem AS, Shahid I, Muhammad A, Muhammad N, Ahmad ZZ, Sven-Erik J (2016) Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Funct Plant Biol 43:632–642CrossRefGoogle Scholar
  129. Zerrouk IZ, Benchabane M, Khelifi L, Yokawa K, Ludwig-Muller J, Baluska F (2016) Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J Plant Physiol 191:111–119CrossRefGoogle Scholar
  130. 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 21:737–744PubMedPubMedCentralCrossRefGoogle Scholar
  131. Zhou C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, Wang J (2016) Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int J Mol Sci 17(6):976.  https://doi.org/10.3390/ijms17060976CrossRefPubMedCentralPubMedGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • F. Pereira
    • 1
  1. 1.Department of MicrobiologyPES’s Ravi Sitaram Naik College of Arts and ScienceFarmagudi, PondaIndia

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