Halotolerant PGPR Bacteria: Amelioration for Salinity Stress

  • Brijendra Kumar Kashyap
  • Roshan Ara
  • Akanksha Singh
  • Megha Kastwar
  • Sabiha Aaysha
  • Jose Mathew
  • Manoj Kumar Solanki


Salinity is one of the major abiotic stresses and brutal environmental factor that adversely affects the productivity of crop and its quality. Approximately 20% of the total cultivated land and 33% of irrigated agricultural lands are oppressed by salinity (salt stress). Agricultural production under elevated salt concentration of soil is highly decreased due to improper nutrition of plants along with osmotic imbalance and drought stress. Salt stress hampers most of the processes including protein synthesis, photosynthesis, growth, and lipid metabolism. In plants, proline amino acid helps in osmotic adjustment, protects macromolecules during dehydration and serves as a scavenger for hydroxyl radical which helps the plants to alleviate the salinity impacts. Under the stressed condition, the tissues of plant are mainly responsible for stunted growth and chlorosis along with nutrient imbalance. Plants like chickpea (Cicer arietinum L.) exposed to saline condition exhibit increased Na+/K+ ratio and decreased uptake of phosphorus (P) in shoot tissue. It has been reported that halotolerant bacteria with genetic diversity may exhibit unique properties like tolerance to the saline condition by various means including synthesis of compatible solutes and biocontrol potential. They improve plant growth under a variety of salinity stress conditions by producing (and regulating) various phytohormones, including indole-3-acetic acid, gibberellic acid, zeatin, abscisic acid, and ethylene, and enhancing phosphate solubilization. The co-inoculation of halotolerant bacteria like Azospirillum, Agrobacterium, Pseudomonas, and several Gram-positive Bacillus is an environment-friendly and economically suited approach for reclaiming salinity-affected lands and maximizing biomass production. In the book chapter, the author will cover the usefulness of various halotolerant bacteria as bioinoculants to improve the soil/plant health against the abiotic stresses.


Abiotic stress Halotolerant bacteria Indole acetic acid PGPR Phytoharmone Salinity 


  1. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci King Saud Univ 26:1–20. Scholar
  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. Scholar
  4. Baniaghil N et al (2013) The effect of plant growth promoting rhizobacteria on growth parameters, antioxidant enzymes and microelements of canola under salt stress. J Appl Environ Biol Sci 3:17–27Google Scholar
  5. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). Following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413. Scholar
  6. Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608. Scholar
  7. Benzon HRL, Rubenecia MRU, Ultra VU Jr, Lee SC (2015) Nano-fertilizer affects the growth, development, and chemical properties of rice. Int JAgronAgric Res 7:2223–7054Google Scholar
  8. Bharti N et al (2014) Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiol Plant 36:45–60. Scholar
  9. 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 6:34768CrossRefGoogle Scholar
  10. Byrt CS, Munns R, Burton RA, Gilliham M, Wege S (2018) Plant science root cell wall solutions for crop plants in saline soils. Plant Sci 269:47–55. Scholar
  11. Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q (2011) Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47:495–506. Scholar
  12. Chen L, Liu Y, Wu G, Njeri KV, Shen Q, Zhang N, Zhang R (2016) Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol Plant 158:34–44. Scholar
  13. Egamberdieva D, Lugtenberg B (2014) Use of plant growth-promoting rhizobacteria to alleviate salinity stress. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, New York. Scholar
  14. Egamberdieva D, Davranov K, Wirth S, Hashem A, Allah EFA (2017) Impact of soil salinity on the plant-growth – promoting and biological control abilities of root associated bacteria. Saudi J Biol Sci 24:1601–1608. Scholar
  15. El-Ramady H, El-Ghamry AM, Mosa A, Alshaal T (2018) Nanofertilizers vs. biofertilizers: new insights. Environ Biodivers Soil Secur 2:40–50. Scholar
  16. Etesami H, Beattie GA (2018) Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front Microbiol 9:148. Scholar
  17. Etesami H, Maheshwari DK (2018) Ecotoxicology and environmental safety use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246. Scholar
  18. Faizan M, Faraz A, Yusuf M, Khan ST, Hayat S (2018) Zinc oxide nanoparticle-mediated changes in photosynthetic efficiency and antioxidant system of tomato plants. Photosynthetica 56:678–686. Scholar
  19. Filomeni G, De Zio D, Cecconi F (2015) Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 22:377–388. Scholar
  20. García-Gutiérrez L, Romera D, Zeriouh H, Perez-Carcia A (2012) Isolation and selection of plant growth-promoting rhizobacteria as inducers of systemic resistance in melon. Plant Soil 358:201–212. Scholar
  21. Gilliham M (2015) Salinity tolerance of crops – what is the cost? Tansley insight salinity tolerance of crops – what is the cost? New Phytol 208:668–673. Scholar
  22. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. Scholar
  23. Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. BioMed Res Int 2016:6284547. Scholar
  24. Hafeez FY, Al Harrasi A, Roberts MR (2015) Suppression of incidence of Rhizoctonia Solani in rice by siderophore producing rhizobacterial strains based on competition for iron. Eur Sci J 11:186–207Google Scholar
  25. Haghighi M, Afifipour Z, Mozafarian M (2012) The effect of N-Si on tomato seed germination under salinity levels. J Biol Environ Sci 6:87–90Google Scholar
  26. Hernández-León R, Rojas-Solis D (2015) Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Control 81:83–92. Scholar
  27. Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1–14. Scholar
  28. Ishitani M (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678. Scholar
  29. Jain M, Mathur G, Koul S, Sarin NB (2001) Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogaea L.). Plant Cell Rep 20:463–468. Scholar
  30. Jalili F, Khavazi K, Pazira E, Nejati A, Rahmani HA, Sadaghiani HR, Miransari M (2009) Isolation and characterization of ACC deaminase- producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674. Scholar
  31. Jha Y, Subramanian RB (2014) PGPR regulate caspase-like activity, programmed cell death, and antioxidant enzyme activity in paddy under salinity. Physiol Mol Biol Plants 20:201–207. Scholar
  32. Jsarotia P, Kashyap PL, Bhardwaj AK, Kumar S (2018) Nanotechnology scope and applications for wheat production and quality enhancement: a review of recent advances. Wheat Barley Res 10.
  33. Kang S, Khan AL, Waqas M, You Y-H, Kim J-H, Kim J-G, Hamaun 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 9:673–682. Scholar
  34. Kumar V (2012) Phosphate solubilizing activity of some bacterial strains isolated from chemical pesticide exposed agriculture soil. Int J Eng Res Dev 3:1–6Google Scholar
  35. Kumar A, Singh VP, Tripathi V, Singh PP, Singh AK (2018) Plant growth promoting rhizobacteria (PGPR): perspective in agriculture under biotic and abiotic stress. In: Agriculture under biotic and abiotic stress, crop improvement through microbial biotechnology. Elsevier B.V. Scholar
  36. LäuchliA, GrattanSR (2011) Plant responses to saline and sodic conditions. In: Wallendar WW, Tanji KK (eds) Agricultural salinity assessment and management. p169–205. doi: Scholar
  37. López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant-Microbe Interact 20:207–217. Scholar
  38. Lutts S, Majerus V, Kinet J (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105:450–458CrossRefGoogle Scholar
  39. Marulanda A, Azcon 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 232:533–543. Scholar
  40. 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. Scholar
  41. Meldau DG, Meldau S, Hoang LH, Underberg S, Wunsche H, Baldwin IT (2013) Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25:2731–2747. Scholar
  42. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986. Scholar
  43. Nasher Mohamed A, Razi Ismail M, Hasan Rahman M (2010) In vitro response from cotyledon and hypocotyls explants in tomato by inducing 6-benzylaminopurine. Afr J Biotechnol 9:4802–4807. Scholar
  44. Nautiyal CS, Srivastava R, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66:1–9. Scholar
  45. Numan M (2018) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32. Scholar
  46. Pandey K, Lahiani MH, Hicks VK, Hudson MK, Green MJ, Khodakovskaya M (2018) Effects of carbon-based nanomaterials on seed germination, biomass accumulation and salt stress response of bioenergy crops. PLOS One:1–17.
  47. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15CrossRefGoogle Scholar
  48. Pérez-García A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22:187–193. Scholar
  49. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. Scholar
  50. Porcel R, Zamarreno AM, Carcia-Mina JM, Aroca R (2014) Involvement of plant endogenous ABA in Bacillus megaterium PGPR activity in tomato plants. BMC Plant Biol 14:36. Scholar
  51. Proseus TE, Boyer JS (2012) Pectate chemistry links cell expansion to wall deposition in Chara corallina. Plant Signal Behav 7:1490–1492. Scholar
  52. Qiu M, Zhang R, Xue C (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48:807–816. Scholar
  53. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292. Scholar
  54. Shahzad SM, Khalid A, Arshad M (2010) Screening rhizobacteria containing ACC-deaminase for growth promotion of chickpea seedlings under axenic conditions. Soil Environ 29:38–46Google Scholar
  55. Shainberg I, Levy GJ, Goldstein D, Mamedov AI (2001) Prewetting rate and sodicity effects on the hydraulic conductivity of soils. Aust J Soil Res 39:1279–1291. Scholar
  56. Shao J, Li S, Zhang N, Cui X, Zhou X, Zhang G, Shen Q, Zhang R (2015) Analysis and cloning of the synthetic pathway of the phytohormone indole -3-acetic acid in the plant-beneficial Bacillus amyloliquefaciens SQR9. Microb Cell Factories 14:130. Scholar
  57. Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. PlantCell 14:465–477. Scholar
  58. 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 22:123–131. Scholar
  59. Siddikee MA, Chauhan P, Anandham R, Han G-H (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584. Scholar
  60. Siddikee A, Glick BR, Chauhan PS, Wj Y, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434. Scholar
  61. Siddiqui MH, Al-whaibi MH (2014) Role of nano-SiO 2 in germination of tomato (Lycopersicum esculentum seeds Mill). Saudi J Biol Sci 21:13–17. Scholar
  62. Siddiqui MH, Al-Whaibi MH, Faisal M, Al Sahli AA (2014) Nano-silicon dioxide mitigates the adverse effects of salt stress on Cucurbita pepo L. Environ Toxicol Chem 33:2429–2437. Scholar
  63. Sultana N, Ikeda T, Itoh R (1999) Effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 42:211–220. Scholar
  64. Tabassum B, Khan A, Tariq RM, Ramzan M (2017) Review- bottlenecks in commercialisation and future prospects of PGPR. Appl Soil Ecol 121:102–117. Scholar
  65. Vacheron J, Desbrosses G, Bouffaud M-L, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356CrossRefGoogle Scholar
  66. Vaishnav A, Kumari S, Jain S, Varma A, Choudhary DK (2015) Putative bacterial volatile-mediated growth in soybean (Glycine max L. Merrill) and expression of induced proteins under salt stress. J Appl Microbiol 119:539–551. Scholar
  67. Valetti L, Iriarte L, Fabra A (2018) Growth promotion of rapeseed (Brassica napus) associated with the inoculation of phosphate solubilizing bacteria. Appl Soil Ecol. Scholar
  68. Waskom RM, Bauder T, Davis JG, Andales AA (2012) Diagnosing saline and sodic soil problems, Crop Seris-Soil, Fact Sheet 0.521. Colarodo State University, Fort Collins, pp 1–2Google Scholar
  69. Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166. Scholar
  70. Wu Z, Yue H, Lu J (2012) Characterization of rhizobacterial strain Rs-2 with ACC deaminase activity and its performance in promoting cotton growth under salinity stress. World J Microbiol Biotechnol 28:2383–2393. Scholar
  71. Xu Z, Shao J, Li B, Yan X, Shan Q, Zhang R (2012) Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl Environ Microbiol 79:808–815. Scholar
  72. Yan N, Marschner P, Cao W, Zuo C, Qin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Water Conserv Res 3:316–323. Scholar
  73. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. Scholar
  74. Yao L, 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 46:49–54. Scholar
  75. Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78:5942–5944. Scholar
  76. Zhang L, Tian L-H, Zhao J-F, Song Y, Zhang C-J, Guo Y (2008) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928. Scholar
  77. Zhang H, Liu W, Wan L (2010) Functional analyses of ethylene response factor JERF3 with the aim of improving tolerance to drought and osmotic stress in transgenic rice. Transgenic Res 19:809–818. Scholar
  78. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. Scholar
  79. Zushi K, Matsuzoe N, Kitano M (2009) Developmental and tissue-specific changes in oxidative parameters and antioxidant systems in tomato fruits grown under salt stress. Sci Horticult 122:362–368. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Brijendra Kumar Kashyap
    • 1
  • Roshan Ara
    • 1
  • Akanksha Singh
    • 1
  • Megha Kastwar
    • 1
  • Sabiha Aaysha
    • 1
  • Jose Mathew
    • 1
  • Manoj Kumar Solanki
    • 2
  1. 1.Department of BiotechnologyBundelkhand UniversityJhansiIndia
  2. 2.Department of Food Quality & Safety, Institute for Post-harvest and Food Sciences, The Volcani CenterAgricultural Research OrganizationRishon LeZionIsrael

Personalised recommendations