Skip to main content

Exploring Halotolerant Rhizomicrobes as a Pool of Potent Genes for Engineering Salt Stress Tolerance in Crops

  • Chapter
  • First Online:

Abstract

Soil salinization is a constant threat to crop productivity and ecology worldwide. The conventional approach, breeding salt-tolerant plant cultivars, has often failed to efficiently alleviate this devastating environmental stress factor. In contrast, the use of a diverse array of microorganisms harbored by plants has attracted increasing attention because of the remarkable beneficial effects of them on plants. Among these microorganisms, halophilic and halotolerant rhizomicrobes is one of the most important extremophilic microorganisms. They can be found in saline or hypersaline ecosystems and have developed different adaptations to survive in salty environments. Their proteins and encoding genes are magnificently engineered to function in a milieu containing 2–5 M salt and represent a valuable repository and resource for reconstruction and visualizing processes of habitat selection and adaptive evolution. Indeed, the natural occurrence of these microorganisms in saline soils opens up a possible important role of them in increasing the salt tolerance in crops. They are capable of eliciting physical, chemical, and molecular changes in plants which enhanced their tolerance and promoted their growth, and thus they can refine agricultural practices and production under saline conditions. Likewise, their ability to serve as bioinoculants could be a more ready utilizable and sustainable solution to ameliorate the deleterious salt effects on plants. However, the ecology of their interactions with plants is still under investigation and not fully understood. This chapter aims to introduce the halotolerant rhizomicrobes and shed light on their special mechanisms to adapt to salinity conditions. A special section would be dedicated for their potential to be exploited in engineering salt tolerance in crops.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

AMF:

Arbuscular mycorrhizal fungi

APX:

Ascorbate peroxidase

CAT:

Catalase

DHAR:

Dehydroascorbate reductase

EPS:

Exopolysaccharides

GPX:

Guaiacol peroxidase

GR:

Glutathione reductase

IAA:

Indole acetic acid

LCO:

Lipo-chitooligosaccharide

MDA:

Malondialdehyde

MDHAR:

Monodehydroascorbate reductase

mtlD:

Mannitol 1-phosphate dehydrogenase

PGDH:

3-Phosphoglycerate dehydrogenase

PGPR:

Plant growth-promoting rhizobacteria

QACs:

Quaternary ammonium compounds

ROS:

Reactive oxygen species

SHMT:

Serine hydroxymethyltransferase

SOD:

Superoxide dismutase

SOS:

Salt overly sensitive

VOCs:

Volatile organic compounds

VSP2 :

Vegetative storage protein 2

References

  • 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 44:1341–1348

    Article  PubMed  Google Scholar 

  • Alavi P, Starcher MR, Zachow C, Müller H, Berg G (2013) Root- microbe systems: the effect and mode of interaction of Stress Protecting Agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front Plant Sci 4:141

    Article  PubMed  PubMed Central  Google Scholar 

  • Anwar T, Chauhan RS (2012) Computational analysis of halotolerance gene from halophilic prokaryotes to infer their signature sequences. Int J Adv Biotechnol Bioinforma 1(1):69–78

    Google Scholar 

  • Arora S, Patel P, Vanza M, Pao GG (2014) Isolation and characterization of endophytic bacteria colonizing halophyte and other salt tolerant plant species from Coastal Gujarat. Afr J Microbiol Res 8(17):1779–1788

    Article  Google Scholar 

  • Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Essah PA, Tester M, Very A-A, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 29:379–387

    Article  PubMed  CAS  Google Scholar 

  • 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 6:34768

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bhattacharjee S (2012) The language of reactive oxygen species signaling in plants. J Bot 2012:1–22

    Article  CAS  Google Scholar 

  • Bhise KK, Bhagwat PK, Dandge PB (2017) Plant growth-promoting characteristics of salt tolerant Enterobacter cloacae strain KBPD and its efficacy in amelioration of salt stress in Vigna radiata L. J Plant Growth Regul 39:215–226

    Article  CAS  Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    Article  PubMed  CAS  Google Scholar 

  • Bonfá MRL, Grossman MJ, Piubeli F, Mellado E, Durrant LR (2013) Phenol degradation by halophilic bacteria isolated from hypersaline environments. Biodegradation 24:699–709

    Article  PubMed  CAS  Google Scholar 

  • Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signaling in plants. J Exp Bot 55:225–236

    Article  PubMed  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  PubMed  CAS  Google Scholar 

  • DasSarma S, DasSarma P (2015) Halophiles and their enzymes: negativity put to good use. Curr Opin Microbiol 25:120–126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Detkova EN, Boltyanskaya YV (2007) Osmoadaptation of haloalkaliphilic bacteria: role of osmoregulators and their possible practical application. Microbiology 76:511–522

    Article  CAS  Google Scholar 

  • Edbeib MF, Wahab RA, Huyop F (2016) Halophiles: biology, adaptation, and their role in decontamination of hypersaline environments. World J Microbiol Biotechnol 32:135

    Article  PubMed  CAS  Google Scholar 

  • Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864

    Article  CAS  Google Scholar 

  • 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 5:214

    Article  CAS  Google Scholar 

  • Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1782

    Article  PubMed  CAS  Google Scholar 

  • Fulda S, Mikkat S, Huang F et al (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6:2733–2745

    Article  PubMed  CAS  Google Scholar 

  • Goel D, Singh AK, Yadav V, Babbar SB, Murata N, Bansal KC (2011) Transformation of tomato with a bacterial codA gene enhances tolerance to salt and water stresses. J Plant Physiol 168(11):1286–1294

    Article  PubMed  CAS  Google Scholar 

  • Gong X, Zhang J, Liu JH (2014) A stress responsive gene of Fortunella crassifolia FcSISP functions in salt stress resistance. Plant Physiol Biochem 83:10–19

    Article  PubMed  CAS  Google Scholar 

  • Guasch-Vidal B, Estévez J, Dardanelli MS, Soria-Díaz ME, Fernández de Córdoba F, Balog CIA, Manyani H, Gil-Serrano A, Thomas-Oates J, Hensbergen PJ, Deelder AM, Megías M, Van Brussel AAN (2013) High NaCl concentrations induce the nod genes of Rhizobium tropici CIAT899 in the absence of flavonoid inducers. Mol Plant-Microbe Interact 26:451–460

    Article  PubMed  CAS  Google Scholar 

  • Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35(1):87–123

    Article  PubMed  CAS  Google Scholar 

  • Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. In: Kole C, Michler C, Abbott AG, Hall TC (eds) Transgenic crop plants. Springer, Berlin, pp 67–132

    Chapter  Google Scholar 

  • Joghee NN, Jayaraman G (2016) Biochemical changes induced by salt stress in halotolerant bacterial isolates are media dependent as well as species specific. Prep Biochem Biotechnol 46(1):8–14

    Article  PubMed  CAS  Google Scholar 

  • 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 9:673–682

    Article  CAS  Google Scholar 

  • Karan R, Capes MD, DasSarma S (2012) Function and biotechnology of extremophilic enzymes in low water activity. Aquat Biosyst 8(1):4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kixmuller D, Greie JC (2012) An ATP-driven potassium pump promotes long-term survival of Halobacterium salinarum within salt crystals. Environ Microbiol Rep 4:234–241

    Article  PubMed  CAS  Google Scholar 

  • Kolman MA, Nishi CN, Perez-Cenci M et al (2015) Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation. Life (Basel) 5:102–126

    CAS  Google Scholar 

  • Kolp S, Pietsch M, Galinski EA, Gutschow M (2006) Compatible solutes as protectants for zymogens against proteolysis. Biochim Biophys Acta 1764:1234–1242

    Article  PubMed  CAS  Google Scholar 

  • Kumar M, Choi JY, Kumari N, Pareek A, Kim SR (2015) Molecular breeding in Brassica for salt tolerance: importance of microsatellite (SSR) markers for molecular breeding in Brassica. Front Plant Sci 6:688

    PubMed  PubMed Central  Google Scholar 

  • Kurz M (2008) Compatible solute influence on nucleic acids: many questions but few answers. Saline Syst 4:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lai SJ, Lai MC, Lee RJ, Chen YH, Yen HE (2014) Transgenic Arabidopsis expressing osmolyte glycine betaine synthesizing enzymes from halophilic methanogen promote tolerance to drought and salt stress. Plant Mol Biol 85:429

    Article  PubMed  CAS  Google Scholar 

  • Lanyi JK (1990) Halorhodopsin, a light-driven electrogenic chloride transport system. Physiol Rev 70:319–330

    Article  PubMed  CAS  Google Scholar 

  • Liu XD, Luo YT, Mohamed OA, Liu DY, Wei GH (2014) Global transcriptome analysis of Mesorhizobium alhagi CCNWXJ12-2 under salt stress. BMC Microbiol 14:1

    Article  PubMed  Google Scholar 

  • Liu X, Luo Y, Li Z, Wei G (2016) Functional analysis of PrkA – a putative serine protein kinase from Mesorhizobium alhagi CCNWXJ12-2 – in stress resistance. BMC Microbiol 16:227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Metwali EMR, Soliman HIA, Fuller MP, Al-Zahrani HS, Howladar SM (2015) Molecular cloning and expression of a vacuolar Na+/H+ antiporter gene (AgNHX1) in fig (Ficus carica L.) under salt stress. Plant Cell Tissue Organ Cult 123(2):377–387

    Article  CAS  Google Scholar 

  • Miller G, Susuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  PubMed  CAS  Google Scholar 

  • Moreno ML, Sanchez-Porro C, Piubeli F, Frias L, Garcia MT, Mellado E (2011) Cloning, characterization and analysis of cat and ben genes from the phenol degrading halophilic bacterium Halomonas organivorans. PLoS One 6:e21049

    Article  PubMed Central  CAS  Google Scholar 

  • Munns R, Gilliham M (2015) Salinity tolerance of crops – what is the cost? New Phytol 208:668–673

    Article  PubMed  CAS  Google Scholar 

  • Nakbanpote W, Panitlurtumpai N, Sangdee A, Sakulpone N, Sirisom P, Pimthong A (2014) Salt-tolerant and plant growth-promoting bacteria isolated from Zn/Cd contaminated soil: identification and effect on rice under saline conditions. J Plant Interact 9:379–387

    Article  CAS  Google Scholar 

  • 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):5762–5766

    Article  CAS  Google Scholar 

  • 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 11:113–121

    Google Scholar 

  • Noctor G, Foyer CH (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:1–13

    Article  CAS  Google Scholar 

  • Orhan F (2016) Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz J Microbiol 47:621–627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patel KG, Mandaliya VB, Mishra GP, Dobaria JR, Thankppan R (2016) Transgenic peanut overexpressing mtlD gene confers enhanced salinity stress tolerance via mannitol accumulation and differential antioxidative responses. Acta Physiol Plant 38:181

    Article  CAS  Google Scholar 

  • Paul S, Bag SK, Das S, Harvill ET, Dutta C (2008) Molecular signature of hypersalin adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 9:R70

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Piernik A, Hrynkiewicz K, Wojciechowska A, Szymańska A, 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 63:1–15

    Article  Google Scholar 

  • Piubeli F, Lourdes Moreno M, Kishi LT, Henrique-Silva F, Garcia MT, Mellado E (2015) Phylogenetic profiling and diversity of bacterial communities in the Death Valley, an extreme habitat in the Atacama Desert. Indian J Microbiol 55:392–399

    Article  PubMed  PubMed Central  Google Scholar 

  • Plemenitas A, Lenassi M, Konte T, Kejzar A, Zajc J, Gostincar C, Gunde-Cimerman N (2014) Adaptation to high salt concentrations in halotolerant/halophilic fungi: a molecular perspective. Front Microbiol 5:199

    PubMed  PubMed Central  Google Scholar 

  • Pourbabaee AA, Bahmani E, Alikhani HA, Emami S (2016) Promotion of wheat growth under salt stress by halotolerant bacteria containing ACC deaminase. J Agric Sci Technol 18:855–864

    Google Scholar 

  • Qiu Q, Guo Y, Dietrich M, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quadri I, Hassani II, l’Haridon S, Chalopin M, Hacene H, Jebbar M (2016) Characterization and antimicrobial potential of extremely halophilic archaea isolated from hypersaline environments of the Algerian Sahara. Microbiol Res 186–187:119–131

    Article  PubMed  CAS  Google Scholar 

  • Qurashi AW, Sabri AN (2013) Osmolyte accumulation in moderately halophilic bacteria improves salt tolerance of chickpea. Pak J Bot 45:1011–1016

    CAS  Google Scholar 

  • Rahnama H, Vakilian H, Fahimi H, Ghareyazie B (2011) Enhanced salt stress tolerance in transgenic potato plants (Solanum tuberosum L.) expressing a bacterial mtlD gene. Acta Physiol Plant 33:1521–1532

    Article  CAS  Google Scholar 

  • Rajput L, Imran A, Mubeen F, Hafeez FY (2013) Salt-tolerant PGPR strain Planococcus rifietoensis promotes the growth and yield of wheat (Triticum aestivum) cultivated in saline soil. Pak J Bot 45:1955–1962

    Google Scholar 

  • 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. Springer Plus 2(6):1–7

    Google Scholar 

  • Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e14823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rohban R, Amoozegar MA, Ventosa A (2009) Screening and isolation of halophilic bacteria producing extracellular hydrolyses from Howz Soltan Lake, Iran. J Ind Microbiol Biotechnol 36:333–340

    Article  PubMed  CAS  Google Scholar 

  • Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plant. Curr Opin Biotechnol 26:115–124

    Article  PubMed  CAS  Google Scholar 

  • Saghafi K, Ahmadi J, Asgharzadeh A, Bakhtiari S (2013) The effect of microbial inoculants on physiological responses of two wheat cultivars under salt stress. Int J Adv Biol Biomed Res 4:421–431

    Article  Google Scholar 

  • Sarathambal C, Ilamurugu K (2013) Saline tolerant plant growth promoting diazotrophs from rhizosphere of Bermuda grass and their effect on rice. Indian J Weed Sci 45:80–85

    Google Scholar 

  • Saum SH, Muller V (2008) Regulation of osmoadaptation in the moderate halophile Halobacillus halophilus: chloride, glutamate and switching osmolyte strategies. Saline Syst 4:2014

    Article  CAS  Google Scholar 

  • Selvakumar G, Kim K, Hu S, Sa T (2014) Effect of salinity on plants and the role of arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria in alleviation of salt stress. In: Ahmad P, Wani MR (eds) Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 115–144

    Chapter  Google Scholar 

  • Shabani L, Sabzalian MR, Pour SM (2016) Arbuscular mycorrhiza affects nickel translocation and expression of ABC transporter and metallothionein genes in Festuca arundinacea. Mycorrhiza 26:67–76

    Article  PubMed  CAS  Google Scholar 

  • Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 9:1600

    Google Scholar 

  • 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):1577–1584

    Article  PubMed  CAS  Google Scholar 

  • Siddikee MA, Glick BR, Chauhan PS, Yim WJ, 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):427–434

    Article  PubMed  CAS  Google Scholar 

  • Singh RP, Jha PN (2016) A halotolerant bacterium Bacillus licheniformis HSW-16 augments induced systemic tolerance to salt stress in wheat plant (Triticum aestivum). Front Plant Sci 7:1890

    PubMed  PubMed Central  Google Scholar 

  • Soares MA, Li H, Kowalski KP, Bergen M, Torres MS, White JF (2016) Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biol Invasions 18:2689–2702

    Article  Google Scholar 

  • Soontharapirakkul K, Promden W, Yamada N, Kageyama H, Incharoensakdi A, Iwamoto-Kihara A, Takabe T (2011) Halotolerant cyanobacterium Aphanothece halophytica contains an Na+-dependent F1F0-ATP synthase with a potential role in salt-stress tolerance. J Biol Chem 286(12):10169–10176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorty AM, Meena KK, Choudhary K, Bitla UM, Minhas PS, Krishnani KK (2016) Effect of plant growth promoting bacteria associated with halophytic weed (Psoralea corylifolia L) on germination and seedling growth of wheat under saline conditions. Appl Biochem Biotechnol 180:872–882

    Article  PubMed  CAS  Google Scholar 

  • Subramanian S, Souleimanov A, Smith DL (2016) Proteomic studies on the effects of lipo-chitooligosaccharide and thuricin 17 under unstressed and salt stressed conditions in Arabidopsis thaliana. Front Plant Sci 7:1314

    Article  PubMed  PubMed Central  Google Scholar 

  • Talaat NB (2014) Effective microorganisms enhance the scavenging capacity of the ascorbate-glutathione cycle in common bean (Phaseolus vulgaris L.) plants grown in salty soils. Plant Physiol Biochem 80:136–143

    Article  PubMed  CAS  Google Scholar 

  • Talaat NB (2015a) Effective microorganisms improve growth performance and modulate the ROS-scavenging system in common bean (Phaseolus vulgaris L.) plants exposed to salinity stress. J Plant Growth Regul 34:35–46

    Article  CAS  Google Scholar 

  • Talaat NB (2015b) Effective microorganisms modify protein and polyamine pools in common bean (Phaseolus vulgaris L.) plants grown under saline conditions. Sci Hortic 190:1–10

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2011) Influence of arbuscular mycorrhizae on yield, nutrients, organic solutes, and antioxidant enzymes of two wheat cultivars under salt stress. J Plant Nutr Soil Sci 174:283–291

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-stressed wheat (Triticum aestivum L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35:2601–2610

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2014a) Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 98:20–31

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2014b) Modulation of the ROS-scavenging system in salt-stressed wheat plants inoculated with arbuscular mycorrhizal fungi. J Plant Nutr Soil Sci 177:199–207

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2015) Plant-microbe interaction and salt stress tolerance in plants. In: Wani SH, Hossain MA (eds) Managing salt tolerance in plants: molecular and genomic perspectives. CRC Press/Taylor & Francis Group, Oxford, pp 267–289

    Chapter  Google Scholar 

  • Talaat NB, Ghoniem AE, Abdelhamid MT, Shawky BT (2015a) Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress. Plant Growth Regul 75:281–295

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT, Ibrahim AS (2015b) Alleviation of drought induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environ Exp Bot 113:47–58

    Article  CAS  Google Scholar 

  • Tani C, Sasakawa H (2003) Salt tolerance of Casuarina equisetifolia and Frankia Ceql strain isolated from the root nodules of C. equisetifolia. Soil Sci Plant Nutr 49:215–222

    Article  Google Scholar 

  • Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58

    Article  CAS  Google Scholar 

  • Tasseva G, Richard L, Zachowski A (2004) Regulation of phosphatidylcholine biosynthesis under salt stress involves choline kinases in Arabidopsis thaliana. FEBS Lett 566:115–120

    Article  PubMed  CAS  Google Scholar 

  • 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 47:907–916

    Article  CAS  Google Scholar 

  • Trivedi R (2017) Ecology of saline soil microorganisms. In: Arora S, Singh AK, Singh YP (eds) Bioremediation of salt affected soils: an Indian perspective. Springer, Cham, pp 157–172

    Chapter  Google Scholar 

  • Ullah S, Bano A (2015) Isolation of PGPRs from rhizospheric soil of halophytes and its impact on maize (Zea mays L.) under induced soil salinity. Can J Microbiol 11:1–7

    Google Scholar 

  • Vannier N, Mony C, Bittebière AK, Vandenkoornhuyse P (2015) Epigenetic mechanisms and microbiota as a toolbox for plant phenotypic adjustment to environment. Front Plant Sci 6:1159

    Article  PubMed  PubMed Central  Google Scholar 

  • Waditee R, Bhuiyan NH, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T (2005) Proc Natl Acad Sci USA 102:1318–1323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waditee R, Bhuiyan NH, Hirata E, Hibino T, Tanaka Y, Shikata M, Takabe T (2007) Metabolic engineering for betaine accumulation in microbes and plants. J Biol Chem 282(47):34185–34193

    Article  PubMed  CAS  Google Scholar 

  • Waditee R, Sittipol D, Tanaka Y, Takabe T (2012) Overexpression of serine hydroxymethyltransferase from halotolerant cyanobacterium in Escherichia coli results in increased accumulation of choline precursors and enhanced salinity tolerance. FEMS Microbiol Lett 333:46–53

    Article  CAS  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Liang Z, Wen X, Lu C (2008) Genetic engineering of the biosynthesis of glycine betaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86

    Article  PubMed  CAS  Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Yi L (2013) Stability of halophilic proteins: from dipeptide attributes to discrimination classifier. Int J Biol Macromol 53:1–6

    Article  PubMed  CAS  Google Scholar 

  • Zhong NQ, Han LB, Wu XM, Wang LL, Wang F, Ma YH, Xia GX (2012) Ectopic expression of a bacterium NhaD-type Na+/H+ antiporter leads to increased tolerance to combined salt/alkali stresses. J Integr Plant Biol 54(6):412–421

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Wang H, Huang Y, Fang T (2016) Characterization of pyrene degradation by halophilic Thalassospira sp. strain TSL5-1 isolated from the coastal soil of Yellow Sea, China. Int Biodeterior Biodegrad 107:62–69

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Talaat, N.B. (2018). Exploring Halotolerant Rhizomicrobes as a Pool of Potent Genes for Engineering Salt Stress Tolerance in Crops. In: Kumar, V., Wani, S., Suprasanna, P., Tran, LS. (eds) Salinity Responses and Tolerance in Plants, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-90318-7_3

Download citation

Publish with us

Policies and ethics