Advertisement

Microorganisms Aiding Existence and Efficiency of Plants in Saline Environment: What We Know and What to Expect

  • Usha Chakraborty
  • Swarnendu Roy
  • Bishwanath Chakraborty
Chapter
Part of the Soil Biology book series (SOILBIOL, volume 56)

Abstract

Salinity poses a major threat to agriculture and hence to food production globally. Though a number of plants are halophytes, surviving in saline environment and, in some cases, requiring a saline soil for growth, none of the cultivated crops are halophytes. Microorganisms, being ubiquitous, are present everywhere, and a large number of salt-tolerant microbes have been found to be associated with halophytes. Many of them are involved in providing tolerance to the plants against salt stress through various mechanisms such as adjusting osmotic balance, ion homeostasis, enhancing antioxidant machinery for scavenging the toxic reactive oxygen species and production of hormones, etc. The use of beneficial microorganisms which have the potential for plant growth promotion as well as salt stress alleviation is gaining momentum. The most commonly used are the plant growth-promoting bacteria of genus Bacillus, as well as some arbuscular mycorrhizal fungi, particularly belonging to the genus Glomus. This approach would provide a cost-efficient, eco-friendly means of salt stress alleviation linked with plant growth promotion, which in turn could lead to sustainable agriculture under changing climatic conditions.

Keywords

Salinity Halophytes Salt-tolerant microbes Rhizosphere PGPR Mycorrhiza 

References

  1. 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 44:1341–1348PubMedCrossRefGoogle Scholar
  2. Aliasgharzadeh N, Saleh Rastin N, Towfighi H, Alizadeh A (2001) Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 11:119–122CrossRefGoogle Scholar
  3. Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816PubMedCrossRefGoogle Scholar
  4. Arora N, Bhardwaj R, Sharma P, Arora HK (2008) Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress. Acta Physiol Plant 30:833–839CrossRefGoogle Scholar
  5. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639CrossRefGoogle Scholar
  6. Aslam F, Ali B (2018) Halotolerant bacterial diversity associated with Suaeda fruticosa (L.) Forssk. improved growth of maize under salinity stress. Agronomy 8:131.  https://doi.org/10.3390/agronomy8080131 CrossRefGoogle Scholar
  7. Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, Deutsch EW, Shannon P, Chiu Y, Sting Weng R, Richie Gan R, Hung P, Date SV, Marcotte E, Hood L, Ng WV (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead sea. Genome Res 14:2221–2234PubMedPubMedCentralCrossRefGoogle Scholar
  8. Barua S, Tripathi S, Chakraborty A, Ghosh S, Chakrabarti K (2012) Characterization and crop production efficiency of diazotrophic bacterial isolates from coastal saline soils. Microbiol Res 167:95–102PubMedCrossRefGoogle Scholar
  9. 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 32:265–272CrossRefGoogle Scholar
  10. 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 Microbiol Biotechnol 29:379–387PubMedCrossRefGoogle Scholar
  11. Bibi F, Strobel GA, Naseer MI, Yasir M, Al-Ghamdi AAK, Azhar EI (2018) Microbial flora associated with the halophyte – Salsola imbricate and its biotechnical potential. Front Microbiol 9:65.  https://doi.org/10.3389/fmicb2018.00065 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon “Haloquadratum walsbyi”: life at the limits of water activity. BMC Genet 7:169CrossRefGoogle Scholar
  13. Cardinale M, Ratering S, Suarez C, Montoya AMZ, Geissler-Plaum R, Schnell S (2015) Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiol Res 181:22–32PubMedCrossRefGoogle Scholar
  14. Carvalho LM, Correia PH, Martins-Loucao A (2001) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170CrossRefGoogle Scholar
  15. Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chakraborty U, Pradhan B (2012) Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Braz J Plant Physiol 24:117–130CrossRefGoogle Scholar
  17. Chakraborty U, Pradhan B (2013) Drought stress-induced oxidative stress and antioxidative responses in four wheat (Triticum aestivum L.) varieties. Arch Agron Soil Sci 58:617–630CrossRefGoogle Scholar
  18. Chakraborty U, Chakraborty BN, Basnet M, Chakraborty AP (2009) Evaluation of Ochrobactrum anthropi TRS-2 and its talc based formulation for enhancement of growth of tea plants and management of brown root rot disease. J Appl Microbiol 107:625–634PubMedCrossRefGoogle Scholar
  19. Chakraborty U, Roy S, Chakraborty AP, Dey P, Chakraborty BN (2011) Plant growth promotion and amelioration of salinity stress in crop plants by a salt-tolerant bacterium. Rec Res Sci Technol 3:61–70Google Scholar
  20. Chakraborty U, Chakraborty BN, Chakraborty AP, Dey PL (2013) Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J Microbiol Biotechnol 29:789–803PubMedCrossRefGoogle Scholar
  21. Chen Y, Chen C, Tan Z, Liu J, Zhuang L, Yang Z, Huang B (2016) Functional identification and characterization of genes cloned from halophyte seashore Paspalum conferring salinity and cadmium tolerance. Front Plant Sci 7:102PubMedPubMedCentralGoogle Scholar
  22. Cheng T, Chen J, Zhang J, Shi S, Zhou Y, Lu L, Wang P, Jiang Z, Yang J, Zhang S, Shi J (2015) Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse response pathways critical for high salinity tolerance. Front Plant Sci 6:30PubMedPubMedCentralGoogle Scholar
  23. Cherian S, Reddy MP (1999) Salt tolerance in the halophyte Suaeda nudiflora Moq.: effect of NaCl on growth, ion accumulation and oxidative enzymes. Indian J Plant Physiol 5:32–37Google Scholar
  24. Chung EJ, Park JE, Jeon CO, Chung YR (2015) Gynuella sunshinyii gen. nov., sp. nov., an antifungal rhizobacterium isolated from a halophyte, Carex scabrifolia Steud. Int J Syst Evol Microbiol 65:1038–1043PubMedCrossRefGoogle Scholar
  25. de Araujo SAM, Silveira JAG, Almeida TD, Rocha IMA, Morais DL, Viegas RA (2006) Salinity tolerance of halophyte Atriplex nummularia L. grown under increasing NaCl levels. J Agric Environ Eng 10:848–854Google Scholar
  26. Debez A, Chaibi W, Bouzid S (2001) Effect of NaCl and growth regulators on germination of Atriplex halimus L. Cahiers Agric 10:135–138Google Scholar
  27. Del Vecchio S, Prisco I, Acosta AT, Starrisci A (2015) Changes in plant species composition of coastal dune habitats over a 20 year period. AoB Plants 7:plv018.  https://doi.org/10.1093/aobpla/plv018 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428PubMedCrossRefGoogle Scholar
  29. English JP, Colmer TD (2013) Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Funct Plant Biol 40:897–912CrossRefGoogle Scholar
  30. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280PubMedPubMedCentralCrossRefGoogle Scholar
  31. Falb M, Pfeiffer F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 15:1336–1343PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fan P, Chen D, He Y, Zhou Q, Tian Y, Gao L (2016) Alleviating salt stress in tomato seedlings using Arthrobacter and Bacillus megaterium isolated from the rhizosphere of wild plants grown on saline-alkaline lands. Int J Phytoremediation 18:1113–1121PubMedCrossRefGoogle Scholar
  33. Feng J, Wang J, Fan P, Jia W, Nie L, Jiang P, Chen X, Lv S, Wan L, Chang S, Li S, Li Y (2015) High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea. BMC Plant Biol 15:63PubMedPubMedCentralCrossRefGoogle Scholar
  34. Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331PubMedPubMedCentralCrossRefGoogle Scholar
  35. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121CrossRefGoogle Scholar
  36. Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–337CrossRefGoogle Scholar
  37. Flowers TJ, Galal HK, Bromham L (2010a) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612CrossRefGoogle Scholar
  38. Flowers TJ, Gaur PM, Gowda CLL, Krisnamurthy L, Samineni S, Siddique KH, Turner NC, Vadez V, Varshney RK, Colmer TD (2010b) Salt sensitivity in chickpea. Plant Cell Environ 33:490–509PubMedCrossRefGoogle Scholar
  39. Frosini S, Lardicci C, Balestri E (2012) Global change and response of coastal dune plants to the combined effects of increased sand accretion (burial) and nutrient availability. PLoS One 7:e47561.  https://doi.org/10.1371/journal.pone.0047561 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Fukami J, de la Osa C, Ollero FJ, Megías M, Hungria M (2017) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45:328–339CrossRefGoogle Scholar
  41. Garg N, Manchanda G (2008) Effect of arbuscular mycorrhizal inoculation of salt-induced nodule senescence in Cajanus cajan (pigeon pea). J Plant Gr Reg 27:115–124CrossRefGoogle Scholar
  42. Gharat SA, Parmar S, Tambat S, Vasudevan M, Shaw BP (2016) Transcriptome analysis of the response to NaCl in Suaeda maritima provides an insight into salt tolerance mechanisms in halophytes. PLoS One 11(9):e0163485PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gill SS, Tajrishi M, Madan M, Tuteja N (2013) A DESDbox helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82:1–22PubMedCrossRefGoogle Scholar
  44. Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312PubMedCrossRefGoogle Scholar
  45. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175CrossRefGoogle Scholar
  46. Glenn EP, Brown JJ (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255CrossRefGoogle Scholar
  47. Goswami D, Dhandhukia P, Patel P, Thakker JN (2014) Screening of PGPR from saline desert of Kutch: Growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol Res 169:66–75PubMedCrossRefGoogle Scholar
  48. Grant WD, Larsen H (1989) Group III. Extremely halophilic archaeobacteria order Halobacteriales ord. nov. In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey’s manual of systematic bacteriology. Williams and Wilkins, Baltimore, pp 2216–2233Google Scholar
  49. Gunde-Cimerman N, Ramos J, Plemenitaš A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241PubMedCrossRefGoogle Scholar
  50. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom 701596, 18 p.  https://doi.org/10.1155/2014/701596 CrossRefGoogle Scholar
  51. Gupta KJ, Stoimenova M, Kaiser WM (2005) In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J Exp Bot 56:2601–2609PubMedCrossRefGoogle Scholar
  52. Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Bio Med Res Intern 6284547, 10 p.  https://doi.org/10.1155/2016/6284547 CrossRefGoogle Scholar
  53. Hahm MS, Son JS, Hwang YJ, Kwon DK, Sa-Youl Ghim SY (2017) Alleviation of salt stress in pepper (Capsicum annum L.) plants by plant growth-promoting rhizobacteria. J Microbiol Biotechnol 27:1790–1797PubMedCrossRefGoogle Scholar
  54. Hamdia ABE, Shaddad MAK, 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 44:165–174CrossRefGoogle Scholar
  55. Harisnaut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Salinity effects on antioxidant enzymes in mulberry cultivar. Sci Asia 29:109–113CrossRefGoogle Scholar
  56. He AL, Niu SQ, Zhao Q, Li YS, Gou JY, Gao HJ, Suo SZ, Zhang JL (2018) Induced salt tolerance of perennial ryegrass by a novel bacterium strain from the rhizosphere of a desert shrub Haloxylon ammodendron. Int J Mol Sci 19:469PubMedCentralCrossRefPubMedGoogle Scholar
  57. Hilderbrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H (2001) Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10:175–183CrossRefGoogle Scholar
  58. Ho I (1987) Vesicular-arbuscular mycorrhizae of halophytic grasses in the Alvord desert of Oregon. Northwest Sci 61:148–151Google Scholar
  59. Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768.  https://doi.org/10.3389/fpls.2017.01768 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Indira K, Srinivasan M (2017) Diversity and ecological distribution of endophytic fungi associated with salt marsh plants. Ind J Geo Mar Sci 46:612–623Google Scholar
  61. Jha B, Gontia I, Hartmann A (2011) The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356:265–277CrossRefGoogle Scholar
  62. Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F (2013) Plant growth-promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria x ananassa). Hort Sci 48:563–567CrossRefGoogle Scholar
  63. Kaur A, Devi SR, Vyas P (2018) Stress-tolerant antagonistic plant growth-promoting rhizobacteria from Zea mays. J Plant Prot Res 58:115–123Google Scholar
  64. Kennedy SP, Ng WV, Salzberg SL, Hood L, DasSarma S (2001) Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res 11:1641–1650PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kumar A, Verma JP (2018) Does plant-microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52PubMedCrossRefGoogle Scholar
  66. Kunte HJ (2006) Osmoregulation in bacteria: Compatible solute accumulation and osmosensing. Environ Chem 3:94–99CrossRefGoogle Scholar
  67. Kunte HJ, Trüper HG, Stan-Lotter H (2002) Halophilic microorganisms. In: Horneck G, Baumstark-Khan C (eds) Astrobiology. Springer, BerlinGoogle Scholar
  68. Lai M-C, Hong T-Y, Gunsalus RP (2000) Glycine betaine transport in the obligate halophilic archaeon Methanohalophilus portucalensis. J Bacteriol 182:5020–5024PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276PubMedCrossRefGoogle Scholar
  70. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062PubMedCrossRefGoogle Scholar
  71. Li HQ, Jiang XW (2017) Inoculation with plant growth-promoting bacteria (PGPB) improves salt tolerance of maize seedling. Russ J Plant Physiol 64:235–241CrossRefGoogle Scholar
  72. Li Y, Kong Y, Teng D, Zhang X, He X, Zhang Y, Lv G (2018) Rhizobacterial communities of five co-occurring desert halophytes. Peer J 6:e5508PubMedCrossRefGoogle Scholar
  73. Litchfield CD (1998) Survival strategies for microorganisms in hypersaline environments and their relevance to life on early Mars. Meteorit Planet Sci 33:813–819PubMedCrossRefGoogle Scholar
  74. Liu S, Hao H, Lu X, Zhao X, Wang Y, Zhang Y, Xie Z, Wang R (2017a) Transcriptome profiling of genes involved in induced systemic salt tolerance conferred by Bacillus amyloliquefaciens FZB42 in Arabidopsis thaliana. Sci Rep 7:10795PubMedPubMedCentralCrossRefGoogle Scholar
  75. Liu H, Wang Y, Tang M (2017b) Arbuscular mycorrhizal fungi diversity associated with two halophytes Lycium barbarum L. and Elaeagnus angustifolia L. in Ningxia, China. Arch Agron Soil Sci 63:796–806CrossRefGoogle Scholar
  76. Lv S, Jiang P, Chen X, Fan P, Wang X, Li Y (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol Biochem 51:47–52PubMedCrossRefGoogle Scholar
  77. Ma Y, Galinski EA, Grant WD, Oren A, Ventosa A (2010) Halophiles 2010: life in saline environments. Appl Environ Microbiol 76:6971–6981PubMedPubMedCentralCrossRefGoogle Scholar
  78. Marasco R, Mapelli F, Rolli E, Mosqueira_santillan MJ, Fusi M, Bariselli P, Reddy M, Cherif A, Tsiamis G, Borin S, Daffonchio D (2016) Salicornia strobilacea (synonym of Halocnemum strobilaceum) grown under different tidal regimes selects rhizosphere bacteria capable of promoting plant growth. Front Microbiol 7:1286PubMedPubMedCentralCrossRefGoogle Scholar
  79. 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 232:533–543CrossRefGoogle Scholar
  80. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedCrossRefGoogle Scholar
  81. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  82. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681.  https://doi.org/10.1146/annurev.arplant.59.032607.092911 CrossRefPubMedGoogle Scholar
  83. Muthezhilan R, Sindhuja BS, Hussain AJ, Jayaprakashvel M (2012) Efficiency of plant growth promoting rhizobacteria isolated from sand dunes of Chennai coastal area. Pak J Biol Sci 15:795–799PubMedCrossRefGoogle Scholar
  84. Naidoo G, Rughunanan R (1990) Salt tolerance in the succulent, coastal halophyte, Sarcocornia natalensis. J Exp Bot 41:497–502CrossRefGoogle Scholar
  85. Navarro-Torre S, Barcia-Piedras JM, Mateos-Naranjo E, Redondo-Gomez S, Camacho M, Caviedes MA, Pajuelo E, Rodríguez-Llorente ID (2017) Assessing the role of endophytic bacteria in the halophyte Arthrocnemum macrostachyum salt tolerance. Plant Biol 19:249–256PubMedCrossRefGoogle Scholar
  86. Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, Khan A, AL-Harrasi A (2018) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32CrossRefGoogle Scholar
  87. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedPubMedCentralGoogle Scholar
  88. Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:2PubMedPubMedCentralCrossRefGoogle Scholar
  89. Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:351PubMedPubMedCentralCrossRefGoogle Scholar
  90. Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359PubMedCrossRefGoogle Scholar
  91. 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 374:753–766CrossRefGoogle Scholar
  92. Qin S, Feng W-W, Zhang Y-J, Wang T-T, Xiong Y-W, Xing K (2018) Diversity of bacterial microbiota of coastal halophyte Limonium sinense and amelioration of salinity stress damage by symbiotic plant growth-promoting actinobacterium Glutamicibacter halophytocola KLBMP 5180. Appl Environ Microbiol 84:e01533–e01518PubMedPubMedCentralCrossRefGoogle Scholar
  93. Railsback LB, Ackerly SC, Anderson TF, Cisne JL (1990) Paleontological and isotope evidence for warm saline deep waters in Ordovician oceans. Nature 343:156–159CrossRefGoogle Scholar
  94. Roy S, Chakraborty U (2018) Role of sodium ion transporters and osmotic adjustments in stress alleviation of Cynodon dactylon under NaCl treatment: a parallel investigation with rice. Protoplasma 255:175–191PubMedCrossRefGoogle Scholar
  95. Ruppel S, Franken P, Witzel K (2013) Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct Plant Biol 40:940–951CrossRefGoogle Scholar
  96. Sannazzaro AI, Echeverria M, Albertó EO, Ruiz OA, Menéndez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45:39–46PubMedCrossRefGoogle Scholar
  97. Saum SH, Muller V (2008) Regulation of osmoadaptation in the moderate halophile Halobacillus halophilus: chloride, glutamate and switching osmolyte strategies. Saline Syst 4:4PubMedPubMedCentralCrossRefGoogle Scholar
  98. Schubert S, Neubert A, Schierholt A, Sumer A, Zorb C (2009) Development of salt-resistant maize hybrids: the combination of physiological strategies using conventional breeding methods. Plant Sci 177:196–202CrossRefGoogle Scholar
  99. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pretreated mycorrhizal fungi. J Plant Physiol 164:1144–1151PubMedCrossRefGoogle Scholar
  100. Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600PubMedPubMedCentralGoogle Scholar
  101. Shi-Ying Z, Cong F, Yong-Xia W, Yun-Sheng X, Wei X, Xiao-Long C (2018) Salt-tolerant and plant growth-promoting bacteria isolated from high-yield paddy soil. Can J Microbiol 64:968–978. [Epub ahead of print]CrossRefGoogle Scholar
  102. Siglioccolo A, Paiardini A, Piscitelli M, Pascarella S (2011) Structural adaptation of extreme halophilic proteins through decrease of conserved hydrophobic contact surface. BMC Struct Biol 11:50PubMedPubMedCentralCrossRefGoogle Scholar
  103. Singh RP, Jha PN (2016a) Alleviation of salinity-induced damage on wheat plant by an ACC deaminase-producing halophilic bacterium Serratia sp. SL-12 isolated from a salt lake. Symbiosis 69:101–111.  https://doi.org/10.1007/s13199-016-0387-x CrossRefGoogle Scholar
  104. Singh RP, Jha PN (2016b) The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.). PLoS One 11(6):e0155026PubMedPubMedCentralCrossRefGoogle Scholar
  105. Szymanska S, Płociniczak T, Piotrowska-Seget Z, Hrynkiewicza K (2016) Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L. – community structure and metabolic potential. Microbiol Res 192:37–51PubMedCrossRefGoogle Scholar
  106. Tenchov B, Vescio EM, Sprott GD, Zeidel ML, Mathai JC (2006) Salt tolerance of archaeal extremely halophilic lipid membranes. J Biol Chem 281:10016–10023PubMedCrossRefGoogle Scholar
  107. Tian XY, Zhang CS (2017) Illumina-based analysis of endophytic and rhizosphere bacterial diversity of the coastal halophyte Messerschmidia sibirica. Front Microbiol 8:2288PubMedPubMedCentralCrossRefGoogle Scholar
  108. Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline on salinity tolerance of plants. Appl Soil Ecol 26:143–148CrossRefGoogle Scholar
  109. Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76:115–127PubMedGoogle Scholar
  110. Ullah S, Bano A (2015) Isolation of plant-growth-promoting rhizobacteria from rhizospheric soil of halophytes and their impact on maize (Zea mays L.) under induced soil salinity. Can J Microbiol 61:307–313PubMedCrossRefGoogle Scholar
  111. Ungar I (1991) Ecophysiology of vascular halophytes. CRC, Boca RatonGoogle Scholar
  112. Upadhyay SK, Singh DP (2015) Effect of salt-tolerant plant growth promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol 17:288–293.  https://doi.org/10.1111/plb.12173 CrossRefPubMedGoogle Scholar
  113. Vaishnav A, Varma A, Tuteja N, Choudhary DK (2016) PGPR-mediated amelioration of crops under salt stress. In: Choudhary DK, Varma A, Tuteja N (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 205–226.  https://doi.org/10.1007/978-981-10-2854-0_10 CrossRefGoogle Scholar
  114. Vreeland RH (1987) Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol 14:311–356PubMedCrossRefGoogle Scholar
  115. Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24CrossRefGoogle Scholar
  116. Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137PubMedCrossRefGoogle Scholar
  117. Wilde P, Manal A, Stodden M, Sieverding E, Hilderbrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561PubMedCrossRefGoogle Scholar
  118. Wohlfarth A, Severin J, Galinski EA (1990) The spectrum of compatible solutes in heterotrophic halophilic eubacteria of the family Halomonadaceae. J Gen Microbiol 136:705–712CrossRefGoogle Scholar
  119. Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in coastal vegetation on Okinawa Island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 18:241–249PubMedCrossRefGoogle Scholar
  120. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4PubMedCrossRefGoogle Scholar
  121. Yang A, Akhtar SS, Iqbal S, Amjad M, Naveed M, Zahir ZA, Jacobsen S-E (2016) Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Funct Plant Biol 43:632–642CrossRefGoogle Scholar
  122. Yuan Z, Druzhinina IS, Labbe 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 6:32467.  https://doi.org/10.1038/srep32467 CrossRefPubMedPubMedCentralGoogle Scholar
  123. Zerrouk IZ, Benchabane KL, Yokawa K, Ludwig-Muller J, Baluska F (2016) A 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 191:111–119.  https://doi.org/10.1016/j.jplph.2015.12.009 CrossRefPubMedGoogle Scholar
  124. Zuccarini P, Okurowska P (2008) Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J Plant Nutr 31:497–513CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Usha Chakraborty
    • 1
  • Swarnendu Roy
    • 1
  • Bishwanath Chakraborty
    • 2
  1. 1.Department of Botany, Plant Biochemistry LaboratoryUniversity of North BengalSiliguriIndia
  2. 2.Department of Biological SciencesAliah UniversityKolkataIndia

Personalised recommendations