Skip to main content

Advertisement

SpringerLink
Log in

Endophytic Bacteria in Plant Salt Stress Tolerance: Current and Future Prospects

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Soil salinity is a major limiting factor for crop productivity worldwide and is continuously increasing owing to climate change. A wide range of studies and practices have been performed to induce salt tolerance mechanisms in plants, but their result in crop improvement has been limited due to lack of time and money. In the current scenario, there is increasing attention towards habitat-imposed plant stress tolerance driven by plant-associated microbes, either rhizospheric and/or endophytic. These microbes play a key role in protecting plants against various environmental stresses. Therefore, the use of plant growth-promoting microbes in agriculture is a low-cost and eco-friendly technology to enhance crop productivity in saline areas. In the present review, the authors describe the functionality of endophytic bacteria and their modes of action to enhance salinity tolerance in plants, with special reference to osmotic and ionic stress management. There is concrete evidence that endophytic bacteria serve host functions, such as improving osmolytes, anti-oxidant and phytohormonal signaling and enhancing plant nutrient uptake efficiency. More research on endophytes has enabled us to gain insights into the mechanism of colonization and their interactions with plants. With this information in mind, the authors tried to solve the following questions: (1) how do benign endophytes ameliorate salt stress in plants? (2) What type of physiological changes incur in plants under salt stress conditions? And (3), what type of determinants produced by endophytes will be helpful in plant growth promotion under salt stress?

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abd_Allah EF, Alqarawi AA, Hashem A, Radhakrishnan R, Al-Huqail AA, Al-Otibi FOLN, Malik JA, Alharbi RI, Egamberdieva D (2018) Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defense mechanisms. J Plant Int 13:37–44

    CAS  Google Scholar 

  • Ali S, Charles TC, Glick BR (2012) Delay of flower senescence by bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate deaminase. J Appl Microbiol 113:1139e1144

    Article  CAS  Google Scholar 

  • Ali S, Charles TC, Glick BR (2014a) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Duan J, Charles TC, Glick BR (2014b) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Charles TC, Glick BR (2017) Endophytic phytohormones and their role in plant growth promotion. In: Doty SL (ed) Functional importance of the plant microbiome. Springer, Berlin, pp 89–105. https://doi.org/10.1007/978-3-319-65897-1_6

    Chapter  Google Scholar 

  • Barnawal D, Bharti N, Tripathi A, Pandey SS, Chanotiya CS, Kalra A (2016) ACC-deaminase-producing endophyte Brachybacterium paraconglomeratum strain SMR20 ameliorates chlorophytum salinity stress via altering phytohormone generation. J Plant Growth Regul 35(2):553–564

    Article  CAS  Google Scholar 

  • Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of micro-organisms in agriculture. Appl Microbiol Biotechnol 84:11–18

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215e229

    Article  CAS  Google Scholar 

  • Berthomieu P, Conej ´ero G, Nublat A, Brackenbury WJ, Lambert C et al (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhore SJ, Nithaya R, Loh CY (2010) Screening of endophytic bacteria isolated from leaves of Sambung Nyawa [Gynura procumbens (Lour.) Merr.] for cytokinin-like compounds. Bioinformation 5:191–197

    Article  PubMed  PubMed Central  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  CAS  PubMed  Google Scholar 

  • Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brígido C, Nascimento FX, Duan J, Glick BR, Oliveira S (2013) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Mesorhizobium spp. reduces the negative effects of salt stress in chickpea. FEMS Microbiol Lett 349(1):46–53

    PubMed  Google Scholar 

  • Bulgari D, Casati P, Crepaldi P, Daffonchio D, Quaglino F, Brusetti L, Bianco PA (2011) Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl Environ Microbiol 77:5018–5022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Bauske EM, Musson G, Rodriguez-Kibana R, Kloepper JW (1995) Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol Control 5:83–91

    Article  Google Scholar 

  • Chen L, Dodd IC, Theobald JC, Belimov AA, Davies WJ (2013) The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. J Exp Bot 64:1565–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Hawighorst P, Sun J, Polle A (2014) Salt tolerance in Populus: significance of stress signaling networks, mycorrhization, and soil amendments for cellular and whole-plant nutrition. Env Exp Bot 107:113–124

    Article  CAS  Google Scholar 

  • Cheng Z, Woody OZ, McConkey BJ, Glick BR (2012) Combined effects of the plant growth-promoting bacterium Pseudomonas putida UW4 and salinity stress on the Brassica napus proteome. Appl Soil Ecol 61:255–263

    Article  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choe YH, Kim YS, Kim IS, Bae MJ, Lee EJ, Kim YH, Park HM, Yoon HS (2013) Homologous expression of gamma-glutamylcysteine synthetase increases grain yield and tolerance of transgenic rice plants to environmental stresses. J Plant Physiol 170:610–618

    Article  CAS  PubMed  Google Scholar 

  • Choudhary DK (2012) Microbial rescue to plant under habitat imposed abiotic and biotic stresses. Appl Microbiol Biotechnol 96:1137–1155

    Article  CAS  PubMed  Google Scholar 

  • 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 35:276–300

    Article  CAS  Google Scholar 

  • Choudhary DK, Sharma AK, Agarwal P, Varma A, Tuteja N (2017) Volatiles and food security. Springer, Singapore

    Book  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Ait Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacte- rium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685e1693

    Google Scholar 

  • Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84e93

    Article  CAS  Google Scholar 

  • Compant S, Cl ementC, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Correa-Galeote D, Bedmar EJ, Arone GJ (2018) Maize endophytic bacterial diversity as affected by soil cultivation history. Front Microbiol 9:484

    Article  PubMed  PubMed Central  Google Scholar 

  • Damodaran T, Rai RB, Jha SK, Kannan R, Pandey BK, Sah V, Mishra VK, Sharma DK (2014) Rhizosphere and endophytic bacteria for induction of salt tolerance in gladiolus grown in sodic soils. J Plant Interact 9:577–584

    Article  CAS  Google Scholar 

  • Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R (2005) Control of sodium transport in durum wheat. Plant Physiol 137:807–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Rio L (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837

    Article  CAS  PubMed  Google Scholar 

  • Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P (2015) Endogone, one of the oldest plant-associated fungi, host unique Mollicutes–related endobacteria. New Phytol 205:1464–1472

    Article  CAS  PubMed  Google Scholar 

  • Dias ACF, Costa FEC, Andreote FD, Lacava PT, Teixeira MA, Assumpcão LC, Araújo WL, Azevedo JL, Melo IS (2009) Isolation of micro propagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195

    Article  CAS  Google Scholar 

  • Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22:32–46

    Article  CAS  Google Scholar 

  • Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Shurigin V, Gopalakrishnan S, Sharma R (2014) Growth and symbiotic performance of chickpea (Cicer arietinum) cultivars under saline soil conditions. J Biol Chem Res 31:333–341

    Google Scholar 

  • Egamberdieva D, Jabborova D, Berg G (2016a) Synergistic interactions between Bradyrhizobium japonicum and the endophyte Stenotrophomonas rhizophila and their effects on growth, nodulation and nutrition of soybean under salt stress. Plant Soil 405:35–45

    Article  CAS  Google Scholar 

  • Egamberdieva D, Li L, Lindström K, Räsänen LA (2016b) A synergistic interaction between salt tolerant Pseudomonas and Mezorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress. Appl Microbiol Biotechnol 100:2829–2841

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G (2017) Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol 8:199

    PubMed  PubMed Central  Google Scholar 

  • Etesami H, Alikhani HA (2016) Co-inoculation with endophytic and rhizosphere bacteria allows reduced application rates of N-fertilizer for rice plant. Rhizosphere 2:15

    Article  Google Scholar 

  • FAO (2015) The state of food insecurity in the world 2015. Meeting the 2015 international hunger targets: taking stock of uneven progress. Rome, FAO

  • Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410:335–356

    Article  CAS  Google Scholar 

  • Gagne-Bourque F, Mayer BF, Charron JB, Vali H, Bertrand A, Jabaji S (2015) Accelerated growth rate and increased drought stress resilience of the model grass Brachypodium distachyon colonized by Bacillus subtilis B26. PLoS ONE 10:e0130456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galippe V (1887) Note sur la présence de micro-organismes dans les tissus végétaux. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie et des ses Filiales et Associées 39:410–416

  • Garcia-Orenes F, Morugan-Coronado A, Zornoza R, Scow K (2013) Changes in soil microbial community structure influenced by agricultural management practices in a mediterranean agro-ecosystem. PLoS ONE 8:e80522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, Hardt M, Blom J, Goesmann A, Rothballer M, Hartmann A, Kogel KH (2016) Nonpathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J 10:871

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica Article ID 963401

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2015) Beneficial plant-bacterial interactions. Springer, Heidelberg

    Book  Google Scholar 

  • Gond SK, Bergen MS, Torres MS, White JF Jr (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Seth R, Sharma A (2016) Plant growth-promoting rhizobacteria play a pole as phytostimulators for sustainable agriculture. In: Choudhary DK et al (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 475–493. https://doi.org/10.1007/978-981-10-2854-0_22

    Chapter  Google Scholar 

  • Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang L, Lin M, Yan Y (2015) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25(7):1119–1128

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu P, Zhang W, Xin H, Deng G (2016) Single cell isolation and analysis. Front Cell Dev Biol 4:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768

    Article  PubMed  PubMed Central  Google Scholar 

  • Iniguez AL, Dong Y, Carter HD, Ahmer BMM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant Microbe Interact 18(2):169–178

    Article  CAS  PubMed  Google Scholar 

  • James EK, Gyaneshwar P, Manthan N, Barraquio WL, Reddy PM, Ianetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15:894e906

    Article  Google Scholar 

  • 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 33:797–802

    Article  Google Scholar 

  • 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 anti-oxidative defense systems. Symbiosis 56:77–86

    Article  CAS  Google Scholar 

  • Khan TA, Mazid M, Quddusi S (2014a) Role of organic and inorganic chemicals in plant-stress mitigation. In: Gaur RK, Sharma P (eds) Approaches to plant stress and their management. Springer, Germany, pp 39–52

    Chapter  Google Scholar 

  • Khan AL, Waqas M, Kang S, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HN, Lee I (2014b) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52(8):689–695

    Article  CAS  PubMed  Google Scholar 

  • Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  CAS  PubMed  Google Scholar 

  • Kumari S, Varma A, Tuteja N, Choudhary DK (2016a) Bacterial ACC-deaminase: An eco-friendly strategy to cope abiotic stresses for sustainable agriculture. In: Choudhary DK et al (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 165–185. https://doi.org/10.1007/978-981-10-2854-0_8

    Chapter  Google Scholar 

  • Kumari S, Vaishnav A, Jain S, Varma A, Choudhary DK (2016b) Induced drought tolerance through wild and mutant bacterial strain Pseudomonas simiae in mung bean (Vigna radiata L.). World J Microbiol Biotechnol 32:1–10

    Article  CAS  Google Scholar 

  • Kumari S, Vaishnav A, Jain S, Choudhary DK, Sharma KP (2016c) In vitro screening for salinity and drought stress tolerance in plant growth promoting bacterial strains. Int J Agric Life Sci 2:60–66

    Google Scholar 

  • Lacava PT, Azevedo JL (2013) Endophytic bacteria: a biotechnological potential in agrobiology system. In: Maheshwari D, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin, pp 1–44

    Google Scholar 

  • Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552

    Article  PubMed  PubMed Central  Google Scholar 

  • Lowman JS, Lava-Chavez A, Kim-Dura S, Flinn B, Nowak J, Mei C (2015) Switchgrass field performance on two soils as affected by bacterization of seedlings with Burkholderia phytofirmans strain PsJN. Bioenergy Res 8:440–449

    Article  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Malfanova N, Kamilova F, Validov S, Shcherbakov A, Chebotar V, Tikhonovich I et al (2011) Characterization of Bacillus subtilis HC8, a novel plant-beneficial endophytic strain from giant hogweed. Microbiol Biotechnol 4:523–532

    Article  CAS  Google Scholar 

  • Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D, Borin S (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Res Int. https://doi.org/10.1155/2013/248078

    Article  PubMed  PubMed Central  Google Scholar 

  • Marquez-Santacruz HA, Hernandez-Leon R, Orozco-Mosqueda MC, Velazquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Gen Mol Res 9:2372–2380

    Article  CAS  Google Scholar 

  • Mattos KA, Pádua VL, Romeiro A, Hallack LF, Neves BC, Ulisses TM, Barros CF, Todeschini AR, Previato JO, Mendonça-Previato L (2008) Endophytic colonization of rice (Oryza sativa L.) by the diazotrophic bacterium Burkholderia kururiensis and its ability to enhance plant growth. Anais da Academia Brasileira de Ciências 80:477–493

  • Miliūtė I, Buzaitė O (2011) IAA production and other plant growth promoting traits of endophytic bacteria from apple tree. Biologija 57(2):98–102

    Article  Google Scholar 

  • Mora-Ruiz MD, Font-Verdera F, Orfila A, Rita J, Rosselló-Móra R (2016) Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw145

    Article  Google Scholar 

  • Moya JL, Primo-Millo E, Talon M (1999) Morphological factors determining salt tolerance in citrus seedling: the shoot-to-root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant Cell Environ 22:1425–1433

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Naher UA, Othman R, Shamsuddin ZHJ, Saud HM, Ismail MR (2009) Growth enhancement and root colonization of rice seedlings by Rhizobium and Corynebacterium spp. Int J Agric Biol 11:586–590

    Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2015) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

    Article  CAS  Google Scholar 

  • Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676

    Article  CAS  PubMed  Google Scholar 

  • Okunishi S, Sako K, Mano H, Imamura A, Morisaki H (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microb Environ 20:168e177

    Article  Google Scholar 

  • Pandey PK, Yadav SK, Singh A, Sarma BK, Mishra A, Singh HB (2012) Cross-species alleviation of biotic and abiotic stresses by the endophyte Pseudomonas aeruginosa PW09. J Phytopathol 160:532–539

    Article  Google Scholar 

  • Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199

    Article  CAS  PubMed  Google Scholar 

  • Paungfoo-Lonhienne C, Rentsch D, Robatze S, Webb RI, Sagulenko E, Nasholm T, Schmidt S, Lonhienne TG (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS ONE 5:e11915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pe´rez-Alfocea F, Albacete A, Ghanem ME, Dodd IC (2010) Hormonal regulation of source–sink relations to maintain crop productivity under salinity: a case study of root-to-shoot signaling in tomato. Fun Plant Biol 37:592–603

    Article  Google Scholar 

  • Pliego C, Kamilova F, Lugtenberg B (2011) Plant Growth-promoting bacteria: Fundamentals and exploitation. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Dordrecht, pp 295–343

    Chapter  Google Scholar 

  • Puri A, Padda KP, Chanway CP (2016) Evidence of nitrogen fixation and growth promotion in canola (Brassica napus L.) by an endophytic diazotroph Paenibacillus polymyxa P2b-2R. Biol Fert Soils 52:119–125

    Article  CAS  Google Scholar 

  • Qin S, Zhang YJ, Yuan B, Xu PY, Xing K, Wang J, Jiang JH (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 374:753–766

    Article  CAS  Google Scholar 

  • Qin Y, Druzhinina IS, Pan X, Yuan Z (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol Adv 34:1245–1259

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224

    Article  Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Sci 298:1581–1581

    Article  CAS  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443

    Article  PubMed  Google Scholar 

  • Reiter B, Pfeifer U, Schwab H, Sessitsch A (2002) Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl Environ Microbiol 68(5):2261–2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhodes D, Nadolska-Orczyk A, Rich PJ (2002) Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge U (eds) Salinity: environment, plants, molecules. Springer, Dordrecht, pp 181–204

    Google Scholar 

  • Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114

    Article  CAS  PubMed  Google Scholar 

  • Romero FM, Marina M, Pieckenstain FL (2014) The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Microbiol Lett 351:187–194

    Article  CAS  PubMed  Google Scholar 

  • Rungin S, Indananda C, Suttiviriya P, Kruasuwan W, Jaemsaeng R, Thamchaipenet A (2012) Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek 102:463–472

    Article  CAS  PubMed  Google Scholar 

  • Ruppel S, Franken P, Witzel K (2013) Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct Plant Biol 40:940–951

    Article  CAS  PubMed  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187e1192

    Article  CAS  Google Scholar 

  • Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, Brar D, van Elsas JD (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36

    Article  CAS  PubMed  Google Scholar 

  • Shahzad R, Khan AL, Bilal S, Waqas M, Kang S-M, Lee I-J (2017) Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa.. Environ Exp Bot 136:68–77

    Article  CAS  Google Scholar 

  • Sharma A, Vaishnav A, Jamali H, Srivastava AK, Saxena AK, Srivastava AK (2016) Halophilic bacteria: potential bioinoculant for sustainable agriculture and environment management under salt stress. In: Choudhary DK et al (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 297–325. https://doi.org/10.1007/978-981-10-2854-0_14

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Singh D, Rajawat MVS, Kaushik R, Prasanna R, Saxena AK (2017) Beneficial role of endophytes in biofortification of Zn in wheat genotypes varying in nutrient use efficiency grown in soils sufficient and deficient in Zn. Plant Soil. https://doi.org/10.1007/s11104-017-3189-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Sørensen J, Sessitsch A (2015) Plant-associated bacteria lifestyle and molecular interactions. In: van Elsas JD et al (eds) Modern soil microbiol. 2nd edn. CRC Press, Boca Raton, pp. 211–236

    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  CAS  PubMed  Google Scholar 

  • Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190

    Article  Google Scholar 

  • Sun L, He L, Zhang Y, Zhang W, Wang Q, Sheng X (2008) Isolation and biodiversity of copper-resistant bacteria from rhizosphere soil of Elsholtzia splendens. Wei Sheng Wu Xue Bao 49:1360–1366

    Google Scholar 

  • Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131e136

    Article  CAS  Google Scholar 

  • Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202

    Article  CAS  PubMed  Google Scholar 

  • Tamosiune I, Baniulis D, Stanys V (2017a) Role of endophytic bacteria in stress tolerance of agricultural plants: diversity of micro-organisms and molecular mechanisms. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics in agroecosystem. Springer, Singapore, pp 1–29

    Google Scholar 

  • Tamosiune I, Danas B, Vidmantas S (2017b) Role of endophytic bacteria in stress tolerance of agricultural plants: diversity of micro-organisms and molecular mechanisms. In: Kumar V et al (eds) Probiotics in agroecosystem. Springer. https://doi.org/10.1007/978-981-10-4059-7_1

  • Teh SY, Koh HL (2016) Climate change and soil salinization: impact on agriculture, water and food security. Int J Agric For Plantation 2:1–9

    Google Scholar 

  • Teotia S, Singh D (2014) Oxidative stress in plants and its management. In: Gaur RK, Sharma P (eds) Approaches to plant stress and their management. Springer, Germany, pp 227–253

    Chapter  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian BY, Cao Y, Zhang KQ (2015) Metagenomic insights into communities, functions of endo- phytes, and their associates with infection by root-knot nematode, Meloidogyne incognita, in tomato roots. Sci Rep 5:1–15

    CAS  Google Scholar 

  • Turner N, Colmer T, Quealy J, Pushpavalli R, Krishnamurthy L, Kaur J, Singh G, Siddique KM, Vadez V (2013) Salinity tolerance and ion accumulation in chickpea (Cicer arietinum L.) subjected to salt stress. Plant Soil 365:347–361

    Article  CAS  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants. An overview. Plant Signal Behav 2:79–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaishnav A, Choudhary DK (2018c) Regulation of drought-responsive gene expression in Glycine max l. Merrill is mediated through Pseudomonas simiae strain AU. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9846-3

    Article  Google Scholar 

  • Vaishnav A, Jain S, Kasotia A, Kumari S, Gaur RK, Choudhary DK (2014) Molecular mechanism of benign microbe-elicited alleviation of biotic and abiotic stresses for plants. In: Gaur RK et al (eds) Approaches to plant stress and their management. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1620-9_16

    Chapter  Google Scholar 

  • Vaishnav A, Varma A, Tuteja N, Choudhary DK (2016a) 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 281–295

  • Vaishnav A, Kumari S, Jain S, Varma A, Tuteja N, Choudhary DK (2016b) PGPR mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J Basic Microbiol 56:1–15

    Article  CAS  Google Scholar 

  • Vaishnav A, Hansen AP, Agrawal PK, Varma A, Choudhary DK (2017a) Biotechnological perspectives of Legume–Rhizobium symbiosis. In: Hansen A, Choudhary D, Agrawal P, Varma A (eds) Rhizobium biology and biotechnology. Soil biology, vol 50. Springer, Cham. https://doi.org/10.1007/978-3-319-64982-5_12

    Chapter  Google Scholar 

  • Vaishnav A, Varma A, Tuteja N, Choudhary DK (2017b) Characterization of bacterial volatiles and their impact on plant health under abiotic stress. In: Choudhary D, Sharma A, Agarwal P, Varma A, Tuteja N (eds) Volatiles and food security. Springer, Singapore, pp 15–24

    Chapter  Google Scholar 

  • Vaishnav A, Kasotia A, Choudhary DK (2018a) Role of functional bacterial phylum proteobacteria in Glycine max growth promotion under abiotic stress: a Glimpse on case study. In: Choudhary D, Kumar M, Prasad R, Kumar V (eds) In silico approach for sustainable agriculture. Springer, Singapore, pp 17–49

    Chapter  Google Scholar 

  • Vaishnav A, Sharma SK, Choudhary DK, Sharma KP, Ahmad E, Sharma MP, Ramesh A, Saxena AK (2018b) Nitric oxide as a signaling molecule in plant-bacterial interactions. In: Plant microbiome: stress response. Springer, Singapore, pp 183–199

    Chapter  Google Scholar 

  • Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48(5):559–565

    Article  CAS  PubMed  Google Scholar 

  • Wáskiewicz A, Gładysz O, Goliñski P (2016) Participation of phytohormones in adaptation to salt stress. In: Ahammed GJ, Yu J-Q (eds) Plant hormones under challenging environmental factors. Springer, Dordrecht, pp 75–115

    Google Scholar 

  • Weyens N, Beckers B, Schellingen K, Ceulemans R, Croes S, Janssen J, Haenen S, Witters N, Vangronsveld J (2013) Plant- associated bacteria and their role in the success or failure of metal phytoextraction projects: first observations of a field-related experiment. Microb Biotechnol 6(3):288–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Li X, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056–8061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav J, Verma JP (2014) Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). Eur J Soil Sci 63:70–77

    CAS  Google Scholar 

  • Yaish MW, Al-Harrasi I, Alansari AS, Al-Yahyai R, Glick BR (2017) The use of high throughput DNA sequence analysis to assess the endophytic microbiome of date palm roots grown under different levels of salt stress. Int Microbiol 19:143–155

    Google Scholar 

  • Yuan Z, Druzhinina IS, Labbé J, Redman R, Qin Y, Rodriguez R, Zhang C, Tuskan GA, Lin F (2016) Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci Rep 6:32467

  • Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, Sheng XF (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The first and corresponding author duly acknowledge DBT and SERB-Grant no. BT/PR1231/AGR/21/340/2011 and SR/FT/LS-129/2012 to DKC respectively whereon idea was conceived to write glimpses in this area. Corresponding authors express thanks to co-authors for their contribution to design figures and compilation of review paper very worthy.

Author information

Authors and Affiliations

  1. Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, 221005, India

    Anukool Vaishnav

  2. K. S. Saket PG College (Affiliated to Dr. Ram Manohar Lohia Avadh University, Faizabad, Uttar Pradesh, India), Ayodhya, Faizabad, 224123, India

    Awadhesh K. Shukla

  3. ICAR-National Bureau of Agriculturally Important Microorganisms Kushmaur, Maunath Bhanjan, Uttar Pradesh, 275103, India

    Anjney Sharma

  4. National Centre of Biological Science, Life Science Cluster Campus, Bellary Road, Bangalore, Karnataka, 560065, India

    Roshan Kumar

  5. Amity Institute of Microbial Technology (AIMT), Amity University, Block ‘E-3’, 4th Floor, Sector-125, Noida, Gautam Buddha Nagar, Uttar Pradesh, 201313, India

    Devendra K. Choudhary

Authors
  1. Anukool Vaishnav
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Awadhesh K. Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anjney Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roshan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Devendra K. Choudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Devendra K. Choudhary.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vaishnav, A., Shukla, A.K., Sharma, A. et al. Endophytic Bacteria in Plant Salt Stress Tolerance: Current and Future Prospects. J Plant Growth Regul 38, 650–668 (2019). https://doi.org/10.1007/s00344-018-9880-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-018-9880-1

Keywords

Search

Navigation