3 Biotech

, 9:261 | Cite as

An overview on improvement of crop productivity in saline soils by halotolerant and halophilic PGPRs

  • Davood Saghafi
  • Nasser Delangiz
  • Behnam Asgari Lajayer
  • Manour GhorbanpourEmail author
Review Article


Salinity of water and soil are of the most important factors limiting the production of crops. Moreover, with the increasing population of the planet and saline fields worldwide there is no choice but to use saline soil and water in the near future. Therefore, to increase plant growth under saline stress condition, provision of sustainable and environmentally friendly management for the use of saline water and soil resources is necessary. The development of saline resistant plants is a potent approach to solve this problem. Generally, soil salinity negatively affects the plant growth through ion toxicity, oxidative stress, osmotic stress and ethylene generation. In recent years, scientists through genetic engineering techniques, which are based on molecular and physiological characteristics of plants, have made salt tolerance plants. However, the validation of the present technique is restricted to laboratory condition and it is not easily applied in the agronomy research under field environment. Another option would be to isolate and utilize salinity resistant microorganisms from the rhizosphere of halophyte plants, namely plant growth-promoting rhizobacteria (PGPR). The mechanisms of these bacteria includes; ACC-deaminase and exopolysachared production, osmolite accumulation, antioxidant system activation, ion hemostasis and etc. In this review, we will discuss mechanisms of PGPR in producing tolerate plants under salt stress and how to improve the plant–microbe interactions in future for increasing agricultural productivity to feed all of the world’s people.


Salinity stress Plant growth promoting rhizobacteria (PGPR) Plant–microbe interactions Salt tolerance plants 


Compliance with ethical standards

Conflict of interest

The authors declare that he/she has no conflict of interest.


  1. Abaid-Ullah M, Hassan MN, Jamil M, Brader G, Shah MK, Sessitsch A, Hafeez FY (2015) Plant growth promoting rhizobacteria: an alternate way to improve yield and quality of wheat (Triticum aestivum). Int J Agric Biol 17:51–60Google Scholar
  2. Abeer H, Abdallah EF, Alqarawi AA, Alhuqail AA, Alshalawi SRM, Wirth S, Egamberdieva D (2015) Impact of plant growth promoting bacillus subtilis on growth and physiological parameters of Bassia indica (Indian Bassia) grown under salt stress. Pak J Bot 47(5):1735–1741Google Scholar
  3. Aeron A, Kumar S, Pandey P, Maheshwari DK (2011) Emerging role of plant growth promoting rhizobacteriain agrobiology. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Berlin Heidelberg, pp 1–36Google Scholar
  4. Agarwal DK, Billore SD, Sharma AN, Dupare BU, Srivastava SK (2013a) Soybean: introduction, improvement, and utilization in India: problems and prospects. Agric Res 2(4):293–300CrossRefGoogle Scholar
  5. Agarwal PK, Shukla P, Gupta K, Jha B (2013b) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123PubMedCrossRefPubMedCentralGoogle Scholar
  6. Ahemad M, Khan MS (2011) Functional aspects of plant growth promoting rhizobacteria: recent advancements. Insight Microbiol 1(3):39–54CrossRefGoogle Scholar
  7. Ahmad MS, Zaidi E, Oves AM (2013) Functional aspect of phosphate-solubilizing bacteria: importance in crop production In: Maheshwari DK et al (ed) Bacteria in agrobiology: crop productivityGoogle Scholar
  8. Akhtar SS, Andersen MN, Naveed M, Zahir ZA, Liu F (2015) Interactive effect of biochar and plant growth-promoting bacterial endophytes on ameliorating salinity stress in maize. Funct Plant Biol 42(8):770–781CrossRefGoogle Scholar
  9. Alaghemand A, Khaghani S, Bihamta MR, Gomarian M, Ghorbanpour M (2018) Green synthesis of zinc oxide nanoparticles using Nigella Sativa L. extract: the effect on the height and number of branches. J Nanostruct 8(1):82–88Google Scholar
  10. Alloway BJ (2008) Zinc in soils and crop nutrition. International zinc Association and International Fertilizer Industry Association. Brussels, Belgium and Paris, France, pp 130Google Scholar
  11. Ashraf M, Akram NA (2009) Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Bio technol Adv 6:744–752Google Scholar
  12. Ashraf M, Berge SH, Mahmood OT (2004) Inoculating wheat seedling with exopolysaccharides-producing bacteria restrict sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162Google Scholar
  13. 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 Soil 366(1–2):93–105CrossRefGoogle Scholar
  14. Barker WW, Welch SA, Chu S, Baneld JF (1998) Experimental observations of the effects of bacteria on aluminosilicate weathering. Am Miner 83:1551–1563CrossRefGoogle Scholar
  15. Barnawal D, Singh R, Singh RP (2019) Role of plant growth promoting rhizobacteria in drought tolerance: regulating growthhormones and osmolytes. In: Singh AK, Kumar A, Singh PK (eds) PGPR amelioration in sustainable agriculture. Woodhead Publishing, Cambridge, pp 107–128CrossRefGoogle Scholar
  16. Basu S, Rabara RC, Negi S, Shukla P (2018) Engineering PGPMOs through gene editing and systems biology: a solution for phytoremediation. Trends Biotechnol 1608:1–12Google Scholar
  17. Bélanger RR, Benhamou N, Menzies JG (2003) Cytological evidence of an active role of silicon in wheat resistance to powdery mildew (Blumeria graminis f. sp. tritici). Phytopathology 93:402–412PubMedCrossRefPubMedCentralGoogle Scholar
  18. Ben Rejeb I, Atauri Miranda L, Cordier M, Mauch-Mani B (2013) Induced tolerance and priming for abiotic stress in plants. In: Gaur RK, Sharma P (eds) Molecular approaches in plant abiotic stress. CRC Press, Boca RatonGoogle Scholar
  19. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microb Biotech 29(2):379–387PubMedCrossRefPubMedCentralGoogle Scholar
  20. Biari A, Gholami A, Rahmani HA (2008) Growth promotion and enhanced nutrient uptake of maize (Zea mays L.) by application of plant growth promoting rhizobacteria in arid region of Iran. J Biol Sci 8:1015–1020CrossRefGoogle Scholar
  21. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173(4):677–702PubMedCrossRefPubMedCentralGoogle Scholar
  22. Chakraborty N, Ghosh R, Ghosh S, Narula K, Tayal R, Datta A, Chakraborty S (2013) Reduction of oxalate levels in tomato fruit and consequent metabolic remodeling following overexpression of a fungal oxalate decarboxylase1. Plant Physiol 162(1):364–378PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chaudhary T, Shukla P (2019) Bioinoculants for bioremediation applications and disease resistance: innovative perspectives. Indian J Microbiol 59(2):129–136PubMedCrossRefPubMedCentralGoogle Scholar
  24. Cherif M, Belanger RR (1992) Use of potassium silicate amendments in recirculating nutrient solutions to suppress Pythium ultimum on long english cucumber. J Plant Dis 76(10):1008–1011CrossRefGoogle Scholar
  25. Choudhary DK (2012) Microbial rescue to plant under habitat-imposed abiotic and biotic stresses. Appl Microbiol Biotechnol 96(5):1137–1155PubMedCrossRefPubMedCentralGoogle Scholar
  26. Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2015) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul 35:276–300CrossRefGoogle Scholar
  27. Dubey RS (2005) Photosynthesis in plants under stressful conditions. In: Pessarakli M (ed) Handbook of photosynthesis, 2nd edn. CRC Press, New York, pp 717–718Google Scholar
  28. Egamberdiyeva D (2005) Plant-growth-promoting rhizobacteria isolated from a Calcisol in a semi-arid region of Uzbekistan: biochemical characterization and effectiveness. J Plant Nutr Soil Sci 168(Suppl 1):94–99CrossRefGoogle Scholar
  29. Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase: bacterial traits required in rhizosphere, rhizoplane and/or endophytic competence by beneficial bacteria. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer International, New York, pp 183–258CrossRefGoogle Scholar
  30. Fernandez LA, Zalba P, Gomez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fertil Soil 43:805–809CrossRefGoogle Scholar
  31. Ghorbanpour M, Majnoun-Hoseini N, Rezazadeh SH, Omidi M, Khavazi K, Hatami M (2011) Variations of root and shoot tropane alkaloids production of Hyoscyamus niger under two rhizobacteria strains inoculation and water deficit stress. J Med Plants 10(40):160–170Google Scholar
  32. Ghorbanpour M, Hatami M, Khavazi K (2013) Role of plant growth promoting rhizobacteria on antioxidant enzyme activities and tropane alkaloids production of Hyoscyamus niger under water deficit stress. Turkish J Biol 37:350–360Google Scholar
  33. Ghorbanpour M, Hosseini N, Khodae-Motlagh M, Solgi M (2014) The effects of inoculation with pseudomonads rhizobacteria on growth, quantity andquality of essential oils in sage (Salvia officinalis L.) plant. J Med Plants 52:89–100Google Scholar
  34. Ghorbanpour M, Hatami M, Kariman K, Abbaszadeh Dahaji P (2016) Phytochemical variations and enhanced efficiency of antioxidant and antimicrobial ingredients in Salvia officinalis as inoculated with different rhizobacteria. Chem Biodivers 13:319–330PubMedCrossRefPubMedCentralGoogle Scholar
  35. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39PubMedCrossRefGoogle Scholar
  36. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190(1):63–68PubMedCrossRefGoogle Scholar
  37. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119(3):329–339CrossRefGoogle Scholar
  38. Goswami D, Parmar S, Vaghela H, Dhandhukia P, Thakker J (2015) Describing paenibacillus mucilaginosus strain N3 as an efficient plant growth promoting rhizobacteria (PGPR). Cogent Food Agric 1(1):1000714Google Scholar
  39. Goswami D, Janki N, Pinakin C (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500Google Scholar
  40. Gu MF, Li N, Shao TY, Long XH, Brestič M, Shao HB, Li JB, Mbarki S (2016) Accumulation capacity of ions in cabbage (Brassica oleracea L.) supplied with sea water. Plant Soil Environ 62(7):314–320CrossRefGoogle Scholar
  41. Hall AE (2001) Crop response to environment. CRC Press, New YorkGoogle Scholar
  42. Hemida KA, Reyad AMM (2018) Improvement salt tolerance of safflower plants by endophytic bacteria. J Hortic Plant Res 5:38–56CrossRefGoogle Scholar
  43. Heulin T, Achouak W, Berge O, Normand P, Guinebretière M-H (2002) Paenibacillus graminis sp. nov. and Paenibacillus odorifer sp. nov., isolated from plant roots, soil and food. Int J Syst Evol Microbiol 52:607–616PubMedCrossRefGoogle Scholar
  44. Hiebert FK, Bennett PC (1992) Microbial control of silicate weathering in organic-rich ground water. Science 258:278–281PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hu X, Chen J, Guo J (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22(9):983–990CrossRefGoogle Scholar
  46. Hussain I, Aleti G, Naidu R, Puschenreiter M, Mahmood Q, Rahman MM, Wang F, Shaheen S, Syed JH, Reichenauer TG (2018) Microbe and plant assisted-remediation of organic xenobiotic and its enhancement by genetically modified organisms and recombinant technology: a review. Sci Total Environ 628:1582–1599PubMedCrossRefPubMedCentralGoogle Scholar
  47. Imam J, Singh PK, Shukla P (2016) Plant microbe interactions in post genomic era: perspectives and applications. Front Microbiol 7:1488PubMedPubMedCentralCrossRefGoogle Scholar
  48. Imam J, Singh PK, Shukla P, Mandal NP, Variar M (2017) Microbial interactions in plants: perspectives and applications of proteomics. Curr Protein Pept Sci 18:1–10CrossRefGoogle Scholar
  49. Iqbal N, Umar S, Nazar R (2014) Manipulating osmolytes for breeding salinity-tolerant plants. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crop stress tolerance a sustainable approach. Elsevier Inc., Amsterdam. ISBN 978-0-12-800875-1Google Scholar
  50. Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30(5):435–458CrossRefGoogle Scholar
  51. Jha CK, Saraf M (2015) Plant growth promoting rhizobacteria (PGPR): a review. J Agric Res Dev 5:108–119Google Scholar
  52. 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
  53. Joe MM, Devaraj S, Benson A, Sa T (2016) Isolation of phosphate solubilizing endophytic bacteria from Phyllanthus amarus Schum & Thonn: evaluation of plant growth promotion and antioxidant activity under salt stress. J Appl Res Med Aromatic Plant 3:71–77CrossRefGoogle Scholar
  54. Johnson HE, Broadhurst D, Goodacre R, Smith AR (2003) Metabolic fingerprinting of salt-stressed tomatoes. Phytochemistry 62(6):919–928PubMedCrossRefPubMedCentralGoogle Scholar
  55. Joseph MH, Dhargave TS, Deshpande CP, Srivastava AK (2015) Microbial Solubilisation of Phosphate: pseudomonas versus Trichoderma. Annals of Plant and Soil Research 17:227–232Google Scholar
  56. Karimi E, Aliasgharzad N, Neyshabouri MR, Esfandiari A (2018) Isolation of biofilm formation bacteria from soil and evaluation of their effects on drought stress mediate in wheat plants. Doctoral thesis, faculty of agriculture, Tabriz University, Iran (in Persian with English abstract)Google Scholar
  57. Karthikeyan B, Joe MM, Islam MR, Sa T (2012) ACC deaminase containing diazotrophic endophytic bacteria ameliorate salt stress in Catharanthus roseus through reduced ethylene levels and induction of antioxidative defense systems. Symbiosis 56(2):77–86CrossRefGoogle Scholar
  58. Kasotia A, Varma A, Tuteja N, Choudhary DK (2016) Amelioration of soybean plant from saline-induced condition by exopolysaccharide producing Pseudomonas-mediated expression of high affinity K+-transporter (HKT1) gene. Curr Sci 111(12):25CrossRefGoogle Scholar
  59. Kaushal M, Wani SP (2015) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66:1–8Google Scholar
  60. Khan MS, Zaidi A, Wani PA (2006) Role of phosphate-solubilizing microorganisms in sustainable agriculture – a review. Agron Sustain Dev 27:29–43CrossRefGoogle Scholar
  61. Kiani MZ, Ali A, Sultan T, Ahmad R, Hydar SI (2015) Plant growth promoting rhizobacteria having 1-aminocyclopropane-1-carboxylic acid deaminase to induce salt tolerance in sunflower (Helianthus annus L.). Nat Res 6:391–397Google Scholar
  62. Kim YC, Glick B, Bashan Y, Ryu CM (2013) Enhancement of plant drought tolerance by microbes. In: Aroca R (ed) Plant responses to drought stress. Springer, BerlinGoogle Scholar
  63. Kochian LV (2000) Molecular physiology of mineral nutrient acquisition, transport, and utilization. Biochem Mol Biol Plants 20:1204–1249Google Scholar
  64. Koide RT, Kabir Z (2000) Extra radical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517CrossRefGoogle Scholar
  65. Kumari S, Vaishnav A, Jain S, Varma A, Choudhary DK (2015) Bacterial-mediated induction of systemic tolerance to salinity with expression of stress alleviating enzymes in soybean (Glycinemax L. Merrill). J Plant Growth Regul 34:558–573CrossRefGoogle Scholar
  66. Ladeiro B (2012) Saline agriculture in the 21st century: using salt contaminated resources to cope food requirementsCrossRefGoogle Scholar
  67. Liu X, Luo Y, Li Z, Wang J, Wei G (2017) Role of exopolysaccharide in salt stress resistance and cell motility of Mesorhizobium alhagi CCNWXJ12–2T. Appl Microbiol Biotechnol 101:1–12CrossRefGoogle Scholar
  68. Ma JF, Yamaji N (2006) Silicon uptake and accumulation in lower plants. Trends Plant Sci 11:392–397PubMedCrossRefPubMedCentralGoogle Scholar
  69. Ma Y, Prasad MN, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258PubMedCrossRefPubMedCentralGoogle Scholar
  70. Mah TCF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39PubMedCrossRefPubMedCentralGoogle Scholar
  71. Malinovskaya IM, Kosenko LV, Votselko SK, Podgorskii VS (1990) Role of bacillus mucilaginosus polysaccharide in degradation of silicate minerals. Mikrobiologiya 59:49–55Google Scholar
  72. Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. Biomed Res Int 248078Google Scholar
  73. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedCrossRefPubMedCentralGoogle Scholar
  74. Meena VS, Maurya BR, Bahadur I (2014) Potassium solubilization by bacterial strain in waste mica. Bangladesh J Bot 43(2):235–237CrossRefGoogle Scholar
  75. Metwali EM, Abdelmoneim TS, Bakheit MA, Kadasa NM (2015) Alleviation of salinity stress in faba bean (Vicia faba L.) plants by inoculation with plant growth promoting rhizobacteria (PGPR). Plant Omics 8(5):449Google Scholar
  76. Miller G, Susuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen specieshomeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467CrossRefGoogle Scholar
  77. Minah B, Hazarin Subair F (2015) Isolation and Screening bacterial exopolysaccharide (EPS) from potato rhizosphere in highland and the potential as a producer indole acetic acid (IAA). Procedia Food Science 3:74–81CrossRefGoogle Scholar
  78. Naik PR, Raman G, Narayanan KB, Sakthivel N (2008) Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiol 8(1):230PubMedPubMedCentralCrossRefGoogle Scholar
  79. Nautiyal CS, Govindarajan R, Lavania M, Pushpangadan P (2008) Novel mechanism of modulating natural antioxidants in functional foods: involvement of plant growth promoting rhizobacteria NRRL B-30488. J Agric Food Chem 56(12):4474–4481PubMedCrossRefPubMedCentralGoogle Scholar
  80. Nemat MA, Magdi TA, Magdy A (2012) Ameliorate of environmental salt stress on the growth of Zea mays L. plants by exopolysaccharides producing bacteria. J Appl Sci Res 8(4):2033–2044Google Scholar
  81. Ng LC, Anuar SNA, Jong JW, Elham MSH (2016) Phytobeneficial and plant growth-promotion properties of silicon-solubilising rhizobacteria on the growth and control of rice sheath blight disease. Asian J Plant Sci 15:92–100CrossRefGoogle Scholar
  82. Nguyen KN, Tran TMT, Nguyen TKO, Nguyen H, Kim N (2017) Isolation and characterization of indole acetic acid producing halophilic bacteria from salt affected soil of rice-shrimp farming system in the Mekong Delta, Vietnam. Agric, For Fish 6(3):69–77Google Scholar
  83. Oberson A, Frossard E, Bühlmann C, Mayer J, Mader P, Luscher A (2013) Nitrogen fixation and transfer in grass-clover leys under organic andconventional cropping systems. Plant Soil 371:237CrossRefGoogle Scholar
  84. Orhan F (2016) Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz J Microbiol 47:621–627PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pandey P, Kang SC, Gupta CP, Maheshwari DK (2005) Rhizosphere competent Pseudomonas aeruginosa GRC1 produces characteristic siderophore and enhances growth of Indian mustard (Brassica campestris). Curr Microbiol 51(5):303–309PubMedCrossRefPubMedCentralGoogle Scholar
  86. Parmar P, Sindhu SS (2013) Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J Microbiol Res 3(1):25–31Google Scholar
  87. Patil AD (2013) Alleviating salt stress in crop plants through salt tolerant microbes. International J Sci Res (IJSR) ISSN (Online) 2319–7064Google Scholar
  88. Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752CrossRefGoogle Scholar
  89. Pirhadi M, Enayatizamir N, Motamedi H, Sorkheh K (2016) Screening of salt tolerant sugarcane endophytic bacteria with potassium and zinc for their solubilizing and antifungal activity Biosci. Biotech Res Commun 9(3):530–538Google Scholar
  90. Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and biofilm formation stimulate Chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191PubMedPubMedCentralCrossRefGoogle Scholar
  91. Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149PubMedCrossRefPubMedCentralGoogle Scholar
  92. Rajwar A, Sahgal M, Johri BN (2013) Legume–rhizobia symbiosis and interactions in agro ecosystems. Plant microbe symbiosis: fundamentals and advances. Springer, New Delhi, pp 233–265CrossRefGoogle Scholar
  93. 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 2:1–7. CrossRefGoogle Scholar
  94. Rashid A, Ryan J (2004) Micronutrient constraints to crop production in soils with mediterranean type charac-teristics: a review. J Plant Nutr 27:959–975CrossRefGoogle Scholar
  95. Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050CrossRefGoogle Scholar
  96. Rasouli Sadagiani MH, Sadegi S, Barin M, Sepehr A, Dolati B (2016) Effects of Suilicate solubilizing bacteria on realizing potassium from mica minerals and its uptake by Zea mays L. plants. J Soil Water Sci 78:1–14Google Scholar
  97. Rodrignes FA, Datnoff LE (2005) Silicon and rice disease management. Fitopatologia Brasileira 30:457–469CrossRefGoogle Scholar
  98. Rodrigues MI, Bravo JP, Sassaki FT, Severino FE, Maia IG (2013) The tonoplast intrinsic aquaporin (TIP) sub family of Eucalyptus grandis: characterization of EgTIP2, a root-specific and osmotic stress-responsive gene. Plant Sci 213:106–113PubMedCrossRefPubMedCentralGoogle Scholar
  99. Rojas-Tapias D, Moreno-Galvan A, Pardo-Diaz 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
  100. Saghafi D, Ghorbanpour M, Asgari Lajayer B (2018) Efficiency of Rhizobium strains as plant growth promoting rhizobacteria on morpho-physiological properties of Brassica napus L. under salinity stress. J Soil Sci Plant Nutr 18(1):253–268Google Scholar
  101. Sandhya V, Ali SKZ, Reddy Grover M, Venkateswarlu GB (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26CrossRefGoogle Scholar
  102. Scavino AF, Pedraza RO (2013) The role of siderophores in plant growth-promoting bacteria. In: Maheshwari DK et al (eds) Bacteria in agrobiology: crop productivityCrossRefGoogle Scholar
  103. Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32:237–249CrossRefGoogle Scholar
  104. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS 9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158(3):243–248PubMedCrossRefPubMedCentralGoogle Scholar
  105. 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 22:123–131PubMedCrossRefPubMedCentralGoogle Scholar
  106. Shukla PS, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachis hypogaea L. by the interaction of halotolerant plant growth promoting rhizobacteria. J Plant Growth Regul 31:195–206CrossRefGoogle Scholar
  107. 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(11):1577–1584PubMedCrossRefPubMedCentralGoogle Scholar
  108. Sindhu SS, Dua S, Verma MK, Khandelwal A (2010) Growth promotion of legumes by inoculation of rhizosphere bacteria. In: Khan MS et al (eds) Microbes for legume improvement. CrossRefGoogle Scholar
  109. Singh G, Biswas DR, Marwaha TS (2010) Mobilization of potassium from waste mica by plant growth promoting rhizobacteria and its assimilation by maize (Zea mays) and wheat (Triticum aestivum L.): a hydroponics study under phytotron growth chamber. J Plant Nutr 33(8):1236–1251CrossRefGoogle Scholar
  110. Sonobe K, Hattori T, An P, Tsuji W, Eneji AE, Kobayashi S, Kawamura Y, Tanaka K, Inanaga S (2011) Effect of silicon application on sorghum root responses to water stress. J Plant Nutr 34:71–82CrossRefGoogle Scholar
  111. Subramanian KS, Tenshia V, Jayalakshmi K, Ramachandran V (2009) Role of arbuscular mycorrhizal fungus (Glomus intraradices)—(fungus aided) in zinc nutrition of maize. Agric Biotechnol Sust Dev 1:29–38Google Scholar
  112. Tang X, Mu X, Shao H, Wang H, Brestic M (2014) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Crit Rev Biotechnol 35:1–13Google Scholar
  113. Tariq M, Hameed S, Malik KA, Hafeez FY (2007) Plant root associated bacteria for zinc mobilization in rice. Pak J Bot 39(1):245Google Scholar
  114. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527PubMedPubMedCentralCrossRefGoogle Scholar
  115. Thomine S, Lanquar V (2011) Iron transport and signaling in plants. Transporters and pumps in plant signaling. Springer, Berlin, pp 99–131CrossRefGoogle Scholar
  116. Timmusk S, Islam A Abd, El D, Lucian C, Tanilas T, Kannaste A (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harshenvironments: enhanced biomass production and reduced emissions of stressvolatiles. PLoS One 9:1–13CrossRefGoogle Scholar
  117. Tisdall JM (1994) Possible role of soil microorganisms in aggregation of soils. Plant Soil 159:115–121CrossRefGoogle Scholar
  118. Toro M (2007) Phosphate solubilizing microorganisms in the rhizosphere of native plants from tropical savannas: an adaptive strategy to acid soils? In: Velazquez C, Rodriguez-Barrueco E (eds) Developments in plant and soil sciences. Springer, The Netherlands, pp 249–252Google Scholar
  119. Tyagia S, Mullaa SI, Leea K, Chaea J, Shukla P (2018) VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Crit Rev Biotechnol 38:1277–1296CrossRefGoogle Scholar
  120. Vaishnav A, Ajit V, Narendra T, Devendra K (2017) PGPR-mediated amelioration of crops under salt stress. Block ‘E-3’, 4th Floor, Amity University Campus, Sector-125, Gautam Buddha Nagar, 201313 Noida, Uttar Pradesh, IndiaGoogle Scholar
  121. Vasanthi N, Saleena LM, Raj SA (2012) Silicon in day today life. World Appl Sci J 17:1425–1440Google Scholar
  122. Wang LL, Chen AP, Zhong NQ, Liu N, Wu XM, Wang F (2014) The Thellungiella salsuginea tonoplast aquaporinTsTIP1;2 functions in protection against multiple abiotic stresses. Plant Cell Physiol 55:148–161PubMedCrossRefPubMedCentralGoogle Scholar
  123. 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 43:161–172CrossRefGoogle Scholar
  124. Xin S, Yu G, Sun L, Qiang X, Xu N, Cheng X (2014) Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in the transgenic Arabidopsis and interacts with target proteins. J Plant Res 127:695–708PubMedCrossRefPubMedCentralGoogle Scholar
  125. Yaish MW, Antony I, Glick R (2015) Isolation and characterization of endophytic plant growth promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance. Antonie van Leeuwenhoek 107:1519–1532PubMedCrossRefPubMedCentralGoogle Scholar
  126. Yan K, Shao H, Shao Ch, Chen P, Zhao Sh, Brestic M, Chen X (2013) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35:2867–2878CrossRefGoogle Scholar
  127. Yao LX, Wu ZS, Zheng YY, 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
  128. Zaidi A, Khan MS, Ahemad M, Oves M, Wani PA (2009) Recent advances in plant growth promotion by phosphate-solubilizing microbes. Microb Strat Crop Improve 23–50Google Scholar
  129. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273PubMedCrossRefPubMedCentralGoogle Scholar
  130. Zhang D, Tong J, He X, Xu Z, Xu L, Wei P, Huang Y, Brestic M, Ma H, Shao H (2016) A novel soybean intrinsic protein gene, GmTIP2;3, involved in responding to osmotic stress. Front Plant Sci 6:1237PubMedPubMedCentralGoogle Scholar
  131. Zhang X, Chen L, Wang J, Wang M, Yang S, Zhao C (2018) Photosynthetic acclimation to long-term high temperature and soil drought stress in two spruce species (Picea crassifolia and P. wilsonii) used for afforestation. J For Res 29(2):363–372CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Davood Saghafi
    • 1
  • Nasser Delangiz
    • 2
  • Behnam Asgari Lajayer
    • 1
  • Manour Ghorbanpour
    • 3
    Email author
  1. 1.Department of Soil Science, Faculty of AgricultureUniversity of TabrizTabrizIran
  2. 2.Department of Plant Biotechnology and Breeding, Faculty of AgricultureUniversity of TabrizTabrizIran
  3. 3.Department of Medicinal Plants, Faculty of Agriculture and Natural ResourcesArak UniversityArakIran

Personalised recommendations