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Halotolerant Rhizobacteria: A Promising Probiotic for Saline Soil-Based Agriculture

  • Ankita Alexander
  • Avinash MishraEmail author
  • Bhavanath JhaEmail author
Chapter

Abstract

Soil salinity is a serious threat to sustainable agriculture, and a number of research are going on to improve saline-resistant crops by using various breeding methods and genetic engineering tools. These methods are time-consuming, often face yield penalties, and many other ethical issues. There is a need to explore other more stable, environmentally friendly methods for the sustainable agriculture. Exploration of plant growth-promoting rhizobacteria (PGPR) associated with salt-tolerant plants (halophytes) and their use as probiotics for saline soil agriculture are a promising substitute for classical approaches. Salinity is one of the major abiotic stress reported from arid and semiarid regions which causes a major loss in the agriculture productivity. Halophytes are adapted to the saline environment because of their genetic makeup and associated microbiome. These microbiomes have potential to survive in the saline condition, but they are not thoroughly explored. Several studies showed that bacteria associated with halophytes, directly and indirectly, support the plant growth and yield in saline conditions; thus, these bacteria can be used as probiotics for salt-sensitive plants (glycophytes) grown in the salt-affected area to enhance the productivity. PGPR induce many morphological, physiological, and genetic changes in a plant which compensate the pressure of salt stress. The genetic level changes in plants due to application or the presence of PGPR are known as induced systemic resistance (ISR). PGPR secrete some beneficial elements like organic solutes, siderophores, etc. to survive in harsh conditions. PGPR also help plants to maintain their osmotic pressure and nutrient balance. The presence of PGPR also affects the level of various phytohormones in plants which play a major role in growth, development, and stress response of the plant.

Keywords

Halophytes Salt-sensitive plants Halotolerant PGPR Salinity stress Crop plants 

Notes

Acknowledgment

CSIR-CSMCRI Communication No.: PRIS-42/2018.

References

  1. AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:276PubMedPubMedCentralGoogle Scholar
  2. Abdelwahab RAI, Cherif A, Cristina C, Nabti E (2017) Extracts from seaweeds and Opuntia ficus-indica cladodes enhance diazotrophic-PGPR halotolerance, their enzymatic potential, and their impact on wheat germination under salt stress. PedosphereGoogle Scholar
  3. Ahmad M, Zahir ZA, Nazli F, Akram F, Arshad M, Khalid M (2013) Effectiveness of halo-tolerant, auxin producing Pseudomonas and Rhizobium strains to improve osmotic stress tolerance in mung bean (Vigna radiata L.). Braz J Microbiol 44(4):1341–1348PubMedCrossRefGoogle Scholar
  4. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora-Morphology, Distrib, Funct Ecol Plants 199(5):361–376CrossRefGoogle Scholar
  5. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27(1):84–93PubMedCrossRefGoogle Scholar
  6. Baki GK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23(5):515–521CrossRefGoogle Scholar
  7. Bal HB, Nayak L, Das S, Adhya TK (2013) Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant and Soil:1–13Google Scholar
  8. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45(4):405–413CrossRefGoogle Scholar
  9. Barra PJ, Inostroza NG, Acuña JJ, Mora ML, Crowley DE, Jorquera MA (2016) Formulation of bacterial consortia from avocado (Persea americana Mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress. Appl Soil Ecol 102:80–91CrossRefGoogle Scholar
  10. Bashan Y, Moreno M, Troyo E (2000) Growth promotion of the seawater-irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol Fertil Soils 32(4):265–272CrossRefGoogle Scholar
  11. Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27(3):411–424PubMedCrossRefGoogle Scholar
  12. Blaylock AD (1994) Soil salinity, salt tolerance, and growth potential of horticultural and landscape plants. University of Wyoming, Cooperative Extension Service, Department of Plant, Soil, and Insect Sciences, College of AgricultureGoogle Scholar
  13. Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74(4):874–880PubMedCrossRefGoogle Scholar
  14. Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Abiotic stress in plants-mechanisms and adaptations. InTechGoogle Scholar
  15. Chandler D, Davidson G, Grant W, Greaves J, Tatchell G (2008) Microbial biopesticides for integrated crop management: an assessment of environmental and regulatory sustainability. Trends Food Sci Technol 19(5):275–283CrossRefGoogle Scholar
  16. Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126(1):52–61CrossRefGoogle Scholar
  17. Coleman-Derr D, Tringe SG (2014) Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol 5:283PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cook RJ, Thomashow LS, Weller DM, Fujimoto D, Mazzola M, Bangera G, Kim D-S (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci 92(10):4197–4201PubMedCrossRefGoogle Scholar
  19. de Souza R, Ambrosini A, Passaglia LM (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38(4):401–419PubMedPubMedCentralCrossRefGoogle Scholar
  20. de Souza Vandenberghe LP, Garcia LMB, Rodrigues C, Camara MC, de Melo Pereira GV, de Oliveira J, Soccol CR (2017) Potential applications of plant probiotic microorganisms in agriculture and forestry. AIMS Microbiol 3(3):629–648Google Scholar
  21. Del Río LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55(2):71–81PubMedCrossRefGoogle Scholar
  22. Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22(1):32–46CrossRefGoogle Scholar
  23. Egamberdieva D (2008) Plant growth promoting properties of rhizobacteria isolated from wheat and pea grown in loamy sand soil. Turk J Biol 32(1):9–15Google Scholar
  24. Egamberdieva D (2011) Survival of Pseudomonas extremorientalis TSAU20 and P. chlororaphis TSAU13 in the rhizosphere of common bean (Phaseolus vulgaris) under saline conditions. Plant Soil Environ 57(3):122–127CrossRefGoogle Scholar
  25. Egamberdiyeva D, Höflich G (2004) Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ 56(2):293–301CrossRefGoogle Scholar
  26. El-Tarabily KA, Youssef T (2010) Enhancement of morphological, anatomical and physiological characteristics of seedlings of the mangrove Avicennia marina inoculated with a native phosphate-solubilizing isolate of Oceanobacillus picturae under greenhouse conditions. Plant Soil 332(1–2):147–162CrossRefGoogle Scholar
  27. Essghaier B, Dhieb C, Rebib H, Ayari S, Boudabous ARA, Sadfi-Zouaoui N (2014) Antimicrobial behavior of intracellular proteins from two moderately halophilic bacteria: strain J31 of Terribacillus halophilus and strain M3-23 of Virgibacillus marismortui. J Plant Pathol Microbiol 5(1):1CrossRefGoogle Scholar
  28. FAO (2016) FAO Soil Portal. http://www.fao.org/soils-portal/en/
  29. Fedoroff NV (2010) The past, present and future of crop genetic modification. New Biotechnol 27(5):461–465CrossRefGoogle Scholar
  30. Fu Q, Liu C, Ding N, Lin Y, Guo B (2010) Ameliorative effects of inoculation with the plant growth-promoting rhizobacterium Pseudomonas sp. DW1 on growth of eggplant (Solanum melongena L.) seedlings under salt stress. Agric Water Manag 97(12):1994–2000CrossRefGoogle Scholar
  31. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401.  https://doi.org/10.6064/2012/963401 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39PubMedCrossRefGoogle Scholar
  33. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37(3):395–412CrossRefGoogle Scholar
  34. Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. BioMed Res Int 2016:6284547PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hamdia MAE-S, Shaddad M, 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(2):165–174CrossRefGoogle Scholar
  36. Han S, Yu B, Wang Y, Liu Y (2011) Role of plant autophagy in stress response. Protein Cell 2(10):784–791PubMedPubMedCentralCrossRefGoogle Scholar
  37. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S (2014) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. In: Transgenic crop plants. Springer, pp 67–132Google Scholar
  39. Jha Y, Subramanian R, 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
  40. Kang S-M, Khan AL, Hamayun M, Hussain J, Joo G-J, You Y-H, Kim J-G, Lee I-J (2012) Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J Microbiol 50(6):902PubMedCrossRefPubMedCentralGoogle Scholar
  41. Kang S-M, Khan AL, Waqas M, You Y-H, Kim J-H, Kim J-G, Hamayun M, Lee I-J (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):673–682CrossRefGoogle Scholar
  42. Karlidag H, Esitken A, Yildirim E, Donmez MF, Turan M (2010) 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):34–45CrossRefGoogle Scholar
  43. Karuppasamy K, Nagaraj S, Kathiresan K (2011) Stress tolerant rhizobium enhances the growth of Samanea saman (JECQ) Merr. Afr J Basic Appl Sci 3(6):278–284Google Scholar
  44. Khalid M, Bilal M, Hassani D, Iqbal HM, Wang H, Huang D (2017) Mitigation of salt stress in white clover (Trifolium repens) by Azospirillum brasilense and its inoculation effect. Bot Stud 58(1):5PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kim K, Jang Y-J, Lee S-M, Oh B-T, Chae J-C, Lee K-J (2014) Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by up-regulation of conserved salinity responsive factors in plants. Mol Cells 37(2):109PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kloepper J, Schroth M (1981) Relationship of in vitro antibiosis of plant growth-promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathology 71(10):1020–1024CrossRefGoogle Scholar
  47. Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65(2):245–252CrossRefGoogle Scholar
  48. Krishnan R, Menon RR, Busse H-J, Tanaka N, Krishnamurthi S, Rameshkumar N (2017) Novosphingobium pokkalii sp nov, a novel rhizosphere-associated bacterium with plant beneficial properties isolated from saline-tolerant pokkali rice. Res Microbiol 168(2):113–121PubMedCrossRefGoogle Scholar
  49. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109(35):14058–14062PubMedCrossRefGoogle Scholar
  50. Lippert K, Galinski EA (1992) Enzyme stabilization be ectoine-type compatible solutes: protection against heating, freezing and drying. Appl Microbiol Biotechnol 37(1):61–65CrossRefGoogle Scholar
  51. Ma W, Guinel FC, Glick BR (2003) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69(8):4396–4402PubMedPubMedCentralCrossRefGoogle Scholar
  52. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158PubMedCrossRefPubMedCentralGoogle Scholar
  53. Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D, Borin S (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Res Int 2013:248078PubMedPubMedCentralCrossRefGoogle Scholar
  54. Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232(2):533–543PubMedCrossRefPubMedCentralGoogle Scholar
  55. Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42(6):565–572PubMedCrossRefGoogle Scholar
  56. Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166(2):525–530CrossRefGoogle Scholar
  57. Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50(1):101–136PubMedCrossRefPubMedCentralGoogle Scholar
  58. Mishra A, Tanna B (2017) Halophytes: potential resources for salt stress tolerance genes and promoters. Front Plant Sci 8:829PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mukhtar S, Ishaq A, Hassan S, Mehnaz S, Mirza MS, Malik KA (2017) Comparison of microbial communities associated with halophyte (Salsola stocksii) and non-halophyte (Triticum aestivum) using culture-independent approaches. Pol J Microbiol 66(3):353–364PubMedCrossRefPubMedCentralGoogle Scholar
  60. Munns R, Gilliham M (2015) Salinity tolerance of crops–what is the cost? New Phytol 208(3):668–673PubMedCrossRefGoogle Scholar
  61. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedPubMedCentralCrossRefGoogle Scholar
  62. Nabti E, Sahnoune M, Ghoul M, Fischer D, Hofmann A, Rothballer M, Schmid M, Hartmann A (2010) Restoration of growth of durum wheat (Triticum durum var. waha) under saline conditions due to inoculation with the rhizosphere bacterium Azospirillum brasilense NH and extracts of the marine alga Ulva lactuca. J Plant Growth Regul 29(1):6–22CrossRefGoogle Scholar
  63. Nabti E, Bensidhoum L, Tabli N, Dahel D, Weiss A, Rothballer M, Schmid M, Hartmann A (2014) Growth stimulation of barley and biocontrol effect on plant pathogenic fungi by a Cellulosimicrobium sp. strain isolated from salt-affected rhizosphere soil in northwestern Algeria. Eur J Soil Biol 61:20–26CrossRefGoogle Scholar
  64. Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74(2):533–542CrossRefGoogle Scholar
  65. Nadeem SM, Zahir ZA, Naveed M, Nawaz S (2013) Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. Ann Microbiol 63(1):225–232CrossRefGoogle Scholar
  66. Narula N, Deubel A, Gans W, Behl R, Merbach W (2006) Paranodules and colonization of wheat roots by phytohormone producing bacteria in soil. Plant Soil Environ 52(3):119CrossRefGoogle Scholar
  67. Naz I, Bano A, Ul-Hassan T (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. Afr J Biotechnol 8(21):5762–5768CrossRefGoogle Scholar
  68. Netondo GW, Onyango JC, Beck E (2004) Sorghum and salinity. Crop Sci 44(3):797–805CrossRefGoogle Scholar
  69. Nia SH, Zarea MJ, Rejali F, Varma A (2012) Yield and yield components of wheat as affected by salinity and inoculation with Azospirillum strains from saline or non-saline soil. J Saudi Soc Agric Sci 11(2):113–121Google Scholar
  70. Nishma K, Adrisyanti B, Anusha S, Rupali P, Sneha K, Jayamohan N, Kumudini B (2014) Induced growth promotion under in vitro salt stress tolerance on solanum lycopersicum by fluorescent pseudomonads associated with rhizosphere. IJASER 3:422–430Google Scholar
  71. Orhan F (2016) Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz J Microbiol 47(3):621–627PubMedPubMedCentralCrossRefGoogle Scholar
  72. Palacio-Rodríguez R, Coria-Arellano JL, López-Bucio J, Sánchez-Salas J, Muro-Pérez G, Castañeda-Gaytán G, Sáenz-Mata J (2017) Halophilic rhizobacteria from Distichlis spicata promote growth and improve salt tolerance in heterologous plant hosts. Symbiosis 73(3):179–189CrossRefGoogle Scholar
  73. Patel D, Jha CK, Tank N, Saraf M (2012) Growth enhancement of chickpea in saline soils using plant growth-promoting rhizobacteria. J Plant Growth Regul 31(1):53–62CrossRefGoogle Scholar
  74. Piernik A, Hrynkiewicz K, Wojciechowska A, Szymańska S, Lis MI, Muscolo A (2017) Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress. Arch Agron Soil Sci 63(10):1404–1418CrossRefGoogle Scholar
  75. Podmore C (2009) Irrigation salinity–causes and impacts. Primefact 937(1):1–4Google Scholar
  76. Príncipe A, Alvarez F, Castro MG, Zachi L, Fischer SE, Mori GB, Jofré E (2007) Biocontrol and PGPR features in native strains isolated from saline soils of Argentina. Curr Microbiol 55(4):314–322PubMedCrossRefPubMedCentralGoogle Scholar
  77. Qin S, Zhang Y-J, Yuan B, Xu P-Y, Xing K, Wang J, Jiang J-H (2014) Isolation of ACC deaminase-producing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil 374(1–2):753–766CrossRefGoogle Scholar
  78. Qurashi AW, Sabri AN (2013) Osmolyte accumulation in moderately halophilic bacteria improves salt tolerance of chickpea. Pak J Bot 45:1011–1016Google Scholar
  79. Raheem A, Ali B (2015) Halotolerant rhizobacteria: beneficial plant metabolites and growth enhancement of Triticum aestivum L. in salt-amended soils. Arch Agron Soil Sci 61(12):1691–1705CrossRefGoogle Scholar
  80. Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37(3):255–263CrossRefGoogle Scholar
  81. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149PubMedCrossRefGoogle Scholar
  82. Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. SpringerPlus 2(1):6PubMedPubMedCentralCrossRefGoogle Scholar
  83. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21(3):541–554PubMedCrossRefGoogle Scholar
  84. Roder A, Hoffmann E, Hagemann M, Berg G (2005) Synthesis of the compatible solutes glucosylglycerol and trehalose by salt-stressed cells of Stenotrophomonas strains. FEMS Microbiol Lett 243(1):219–226PubMedCrossRefGoogle Scholar
  85. Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S, Obando M, Rivera D, Bonilla R (2012) Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol 61:264–272CrossRefGoogle Scholar
  86. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124PubMedCrossRefGoogle Scholar
  87. Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28(4):1503–1509PubMedCrossRefGoogle Scholar
  88. Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99PubMedCrossRefGoogle Scholar
  89. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102(5):1283–1292PubMedCrossRefGoogle Scholar
  90. Saslis-Lagoudakis CH, Hua X, Bui E, Moray C, Bromham L (2014) Predicting species’ tolerance to salinity and alkalinity using distribution data and geochemical modelling: a case study using Australian grasses. Ann Bot 115(3):343–351PubMedPubMedCentralCrossRefGoogle Scholar
  91. Seckin B, Sekmen AH, Türkan I (2009) An enhancing effect of exogenous mannitol on the antioxidant enzyme activities in roots of wheat under salt stress. J Plant Growth Regul 28(1):12CrossRefGoogle Scholar
  92. Shin D-S, Park M-S, Jung S, Lee M-S, Lee K-H, Bae K-S, Kim S-B (2007) Plant growth-promoting potential of endophytic bacteria isolated from roots of coastal sand dune plants. J Microbiol Biotechnol 17(8):1361–1368PubMedGoogle Scholar
  93. Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22(2):123–131PubMedCrossRefGoogle Scholar
  94. Siddikee MA, Chauhan PS, Anandham R, Han G-H, 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(11):1577–1584PubMedCrossRefGoogle Scholar
  95. Siddikee MA, Glick BR, Chauhan PS, Jong Yim W, 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(4):427–434PubMedCrossRefGoogle Scholar
  96. Štajner D, Kevrešan S, Gašić O, Mimica-Dukić N, Zongli H (1997) Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol Plant 39(3):441CrossRefGoogle Scholar
  97. Stutz EW, Défago G, Kern H (1986) Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76(2):181–185CrossRefGoogle Scholar
  98. Suárez R, Wong A, Ramírez M, Barraza A, Orozco MC, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant-Microbe Interact 21(7):958–966PubMedCrossRefGoogle Scholar
  99. Suarez C, Cardinale M, Ratering S, Steffens D, Jung S, Montoya AMZ, Geissler-Plaum R, Schnell S (2015) Plant growth-promoting effects of Hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl Soil Ecol 95:23–30CrossRefGoogle Scholar
  100. Szymańska S, Piernik A, Hrynkiewicz K (2013) Metabolic potential of microorganisms associated with the halophyte Aster tripolium L. in saline soils. Ecol Quest 18(1):9–19Google Scholar
  101. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75(3):748–757PubMedCrossRefGoogle Scholar
  102. Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5(1):51–58CrossRefGoogle Scholar
  103. Tewari S, Arora NK (2014) Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions. Curr Microbiol 69(4):484–494PubMedCrossRefGoogle Scholar
  104. Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, Arora DK (2011) Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol Fertil Soils 47(8):907CrossRefGoogle Scholar
  105. Upadhyay SK, Singh DP, Saikia R (2009) Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Curr Microbiol 59(5):489–496PubMedCrossRefGoogle Scholar
  106. Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14(4):605–611PubMedCrossRefGoogle Scholar
  107. Van Loon L (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119(3):243–254CrossRefGoogle Scholar
  108. Vannier N, Mony C, Bittebière A-K, Vandenkoornhuyse P (2015) Epigenetic mechanisms and microbiota as a toolbox for plant phenotypic adjustment to environment. Front Plant Sci 6:1159PubMedPubMedCentralCrossRefGoogle Scholar
  109. Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24(3):263–290PubMedCrossRefGoogle Scholar
  110. Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10(12):615–620PubMedCrossRefGoogle Scholar
  111. Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4PubMedCrossRefPubMedCentralGoogle Scholar
  112. 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(1):49–54CrossRefGoogle Scholar
  113. Yildirim E, Turan M, Ekinci M, Dursun A, Cakmakci R (2011) Plant growth promoting rhizobacteria ameliorate deleterious effect of salt stress on lettuce. Sci Res Essays 6(20):4389–4396CrossRefGoogle Scholar
  114. Yuan Z, Druzhinina IS, Labbé J, Redman R, Qin Y, Rodriguez R, Zhang C, Tuskan GA, Lin F (2016) Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci Rep 6:32467PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yue H, Mo W, Li C, Zheng Y, Li H (2007) The salt stress relief and growth promotion effect of Rs-5 on cotton. Plant Soil 297(1–2):139–145CrossRefGoogle Scholar
  116. Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:98–169Google Scholar
  117. Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch Microbiol 191(5):415–424PubMedCrossRefGoogle Scholar
  118. Zarea M, Hajinia S, Karimi N, Goltapeh EM, Rejali F, Varma A (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146CrossRefGoogle Scholar
  119. Zhou N, Zhao S, Tian CY (2017) Effect of halotolerant rhizobacteria isolated from halophytes on the growth of sugar beet (Beta vulgaris L.) under salt stress. FEMS Microbiol Lett 364(11).  https://doi.org/10.1093/femsle/fnx091
  120. Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53(1):247–273PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.CSIR-Central Salt and Marine Chemicals Research InstituteBhavnagarIndia
  2. 2.Academy of Scientific and Innovative ResearchCouncil of Scientific and Industrial ResearchGhaziabadIndia

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