Skip to main content

Advertisement

Log in

Biotechnological application of plant growth-promoting endophytic bacteria isolated from halophytic plants to ameliorate salinity tolerance of Vicia faba L.

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Salinity is a major problem affecting crop production all over the world. A wide range of adaptation strategies are required to overcome this problem. Endophytic bacteria can build a symbiotic association with their host to improve host plant salt tolerance. In this study, eighteen bacterial endophyte strains were isolated from two native halophytic plants Arthrocnemum macrostachyum and Spergularia marina, and identified as Bacillus, Brevibacillus, Agrobacterium, and Paenibacillus. These endophytic strains exhibit plant growth-promoting activities including phosphate solubilizing, ammonia production, biocontrol of phytopathogen, extracellular enzymatic activities, and indole-3-acetic acid production under normal and salinity stress. A pot experiment was conducted under field conditions to alleviate the harmful effects of soil salinity on bean (Vicia faba L.) by inoculating their seeds with the most potent bacterial isolates Bacillus subtilis (AR5) and Bacillus thuringiensis (BR1). Salinity treatments induced a significant decrease in both growth parameters and metabolic activities, while the activity of antioxidant enzymes and proline content was significantly increased. However, salinity stress induced higher contents of Na+ and decreased contents of N+, P3+, K+, Ca2+, Mg2+, and K+:Na+, it was found that treatment with B. subtilis (AR5) and B. thuringiensis (BR1) individually or in a combination mitigated the effect of salt stress and improved the plant height, shoot dry weights, proline contents, enzymes activities as well enhanced the accumulation of mineral nutrients in shoot plants. Our results concluded that treatment with co-inoculation of B. subtilis (AR5) and B. thuringiensis (BR1) exerted the greatest effect in alleviating the harmful effect of soil salinity stress and can be used as a suitable bio-approach to reclaim salinity-stressed soils.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Abbasi MK, Sharif S, Kazmi M, Sultan T, Aslam M (2011) Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants. Plant Biosyst 145:159–168

    Article  Google Scholar 

  • Abd-Allah EF, Alqarawi AA, Hashem A, Radhakrishnan R, Al-Huqail AA, Al-Otibi FON, 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 Interact 13:37–44

    Article  CAS  Google Scholar 

  • Abdelhamid MT, Shokr MMB, Bekheta MA (2010) Growth, root characteristics, and leaf nutrients accumulation of four Faba Bean (Vicia faba L.) cultivars differing in their broomrape tolerance and the soil properties in relation to salinity. Commun Soil Sci Plant Anal 41:2713–2728

    Article  CAS  Google Scholar 

  • Abeer H, Abd-Allah E, Alqarawi A, El-Didamony G, Alwhibi M, Egamberdieva D, Ahmad P (2014) Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak J Bot 46:2003–2013

    Google Scholar 

  • Abla E, Souad E, Abdelhadi H, Bazdi O, Khadija O (2015) Antagonistic activity of endophytic bacteria isolated from Mentha rotundifolia L. Int J Sci Technol Res 4:36–39

    Google Scholar 

  • Aczel MR (2019) What is the nitrogen cycle and why is it key to life? Front Young Minds 7:41. https://doi.org/10.3389/frym.2019.00041

    Article  Google Scholar 

  • Agami R, Medani R, Abd El-Mola I, Taha R (2016) Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int J Environ Agri Res 2:78

    Google Scholar 

  • Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011) Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 57:578–589

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Ozturk M, Sharma S, Gucel S (2014) Effect of sodium carbonate-induced salinity–alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J Plant Interact 9:460–467

    Article  CAS  Google Scholar 

  • Ait Barka E, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting Rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246

    Article  PubMed  PubMed Central  Google Scholar 

  • Ali S, Charles TC, Glick BR (2014) 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 

  • ALKahtani MDF, Fouda A, Attia KA, Al-Otaibi F, Eid AM, Ewais EE-D, Hijri M, St-Arnaud M, Hassan SE-D, Khan N, Hafez YM, Abdelaal KAA (2020) Isolation and characterization of plant growth promoting endophytic bacteria from desert plants and their application as bioinoculants for sustainable agriculture. Agronomy 10:1325

    Article  CAS  Google Scholar 

  • Almaghrabi OA, Abdelmoneim T, Albishri HM, Moussa TA (2014) Enhancement of maize growth using some plant growth promoting rhizobacteria (PGPR) under laboratory conditions. Life Sci J 11:764–772

    Google Scholar 

  • Arora S, Patel PN, Vanza MJ, Rao G (2014) Isolation and characterization of endophytic bacteria colonizing halophyte and other salt tolerant plant species from coastal Gujarat. Afr J Microbiol Res 8:1779–1788

    Article  Google Scholar 

  • Ashraf M (2004) Photosynthetic capacity and ion accumulation in a medicinal plant henbane (Hyoscyamus niger L.) under salt stress. J Appl Bot 78:91–96

    CAS  Google Scholar 

  • Aşık BB, Turan MA, Çelik H, Katkat AV (2009) Uptake of wheat (Triticum durun cv. Salihli) under conditions of salinity. Asian J Crop Sci 1:87–95

    Article  Google Scholar 

  • Banik A, Dash GK, Swain P, Kumar U, Mukhopadhyay SK, Dangar TK (2019) Application of rice (Oryza sativa L.) root endophytic diazotrophic Azotobacter sp. strain Avi2 (MCC 3432) can increase rice yield under green house and field condition. Microbiol Res 219:56–65

    Article  CAS  PubMed  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 35:553–564

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Tease I (1973) Rapid determination of the proline for tress studies. Plant Soil 85:107–129

    Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107

    Article  CAS  PubMed  Google Scholar 

  • Bienert GP, Chaumont F (2014) Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1840:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546

    Article  CAS  PubMed  Google Scholar 

  • Boulos L (2005) Flora of egypt. Al Hadara Publishing, Cairo

    Google Scholar 

  • Boulos L (2009) Flora of Egypt checklist, revised annotated edition. Al-Hadara Publishing, Cairo, pp 198–201

    Google Scholar 

  • Chebotar VK, Malfanova NV, Shcherbakov AV, Ahtemova GA, Borisov AY, Lugtenberg B, Tikhonovich IA (2015) Endophytic bacteria in microbial preparations that improve plant development (review). Appl Biochem Microbiol 51:271–277

    Article  CAS  Google Scholar 

  • Chen C, Yu R, Owuor ED, Tony Kong AN (2000) Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharmacal Res 23:605

    Article  CAS  Google Scholar 

  • Chen G, Zhu Y, Wang H-Z, Wang S-J, Zhang R-Q (2007) The metabolites of a mangrove endophytic fungus, Penicillium thomi. J Asian Nat Prod Res 9:159–164

    Article  PubMed  Google Scholar 

  • Chen L, Liu Y, Wu G, Veronican Njeri K, Shen Q, Zhang N, Zhang R (2016) Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol Plant 158:34–44

    Article  CAS  PubMed  Google Scholar 

  • Cheng Z, Park E, Glick BR (2007) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Hodgkiss I, Hyde K (2005) Enzyme production by endophytes of Brucea javanica. J Agric Technol 1:55–66

    Google Scholar 

  • Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–961

    Article  CAS  PubMed  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 

  • Dawood MG, Abdelhamid MT, Schmidhalter U (2014) Potassium fertiliser enhances the salt-tolerance of common bean (Phaseolus vulgaris L.). J Hortic Sci Biotechnol 89:185–192

    Article  CAS  Google Scholar 

  • Dhungana SA, Itoh K (2019) Effects of co-inoculation of indole-3-acetic acid-producing and -degrading bacterial endophytes on plant growth. Horticulturae 5:17

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Egamberdieva D, Wirth S, Jabborova D, Räsänen LA, Liao H (2017a) Coordination between Bradyrhizobium and Pseudomonas alleviates salt stress in soybean through altering root system architecture. J Plant Interact 12:100–107

    Article  CAS  Google Scholar 

  • Egamberdieva D, Wirth SJ, Shurigin VV, Hashem A, Abd-Allah EF (2017b) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01887

    Article  PubMed  PubMed Central  Google Scholar 

  • Eid AM, Salim SS, Hassan SE-D, Ismail MA, Fouda A (2019) Role of endophytes in plant health and abiotic stress management. Microbiome in Plant Health and Disease. Springer, pp 119–144

  • Eid AM, Fouda A, Abdel-Rahman MA, Salem SS, Elsaied A, Oelmüller R, Hijri M, Bhowmik A, Elkelish A, Hassan SE (2021) Harnessing bacterial endophytes for promotion of plant growth and biotechnological applications: an overview. Plants 10:935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Esawi MA, Al-Ghamdi AA, Ali HM, Alayafi AA (2019) Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environ Exp Bot 159:55–65

    Article  CAS  Google Scholar 

  • FAO, IFAD, WFP (2015) The state of food insecurity in the World 2015: meeting the 2015 international hunger targets: taking stock of uneven progress. FAO, Rome. Viewed 26 Sept 2016

  • Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188

    Article  Google Scholar 

  • Fouda AH, Hassan SE-D, Eid AM, Ewais EE-D (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Ann Agric Sci 60:95–104

    Article  Google Scholar 

  • Fouda A, Hassan SED, Eid AM, El-Din Ewais E (2019) The interaction between plants and bacterial endophytes under salinity stress. In: Jha S (ed) Endophytes and secondary metabolites. Springer International Publishing, Cham, pp 591–607

    Chapter  Google Scholar 

  • Fouda A, Eid AM, Elsaied A, El-Belely EF, Barghoth MG, Azab E, Gobouri AA, Hassan SE (2021) Plant growth-promoting endophytic bacterial community inhabiting the leaves of Pulicaria incisa (Lam.) DC inherent to arid regions. Plants 10:76

    Article  CAS  PubMed Central  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401. https://doi.org/10.6064/2012/963401 

    Article  PubMed  PubMed Central  Google Scholar 

  • Gothwal R, Nigam V, Mohan M, Sasmal D, Ghosh P (2008) Screening of nitrogen fixers from rhizospheric bacterial isolates associated with important desert plants. Appl Ecol Environ Res 6:101–109

    Article  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  PubMed  Google Scholar 

  • Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int 2016:6284547

    Article  PubMed  PubMed Central  Google Scholar 

  • Hafez AA, Mikkelsen DS (1981) Colorimetric determination of nitrogen for evaluating the nutritional status of rice. Commun Soil Sci Plant Anal 12:61–69

    Article  CAS  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Aldubise A, Egamberdieva D (2015) Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J Plant Interact 10:230–242

    Article  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Al-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01089

    Article  PubMed  PubMed Central  Google Scholar 

  • Hidri R, Barea JM, Mahmoud OM, Abdelly C, Azcón R (2016) Impact of microbial inoculation on biomass accumulation by Sulla carnosa provenances, and in regulating nutrition, physiological and antioxidant activities of this species under non-saline and saline conditions. J Plant Physiol 201:28–41

    Article  CAS  PubMed  Google Scholar 

  • Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2; 1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26:3003–3014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549

    Article  CAS  Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crop Res 65:151–164

    Article  Google Scholar 

  • Irizarry I, White J (2017) Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol 122:1110–1120

    Article  CAS  PubMed  Google Scholar 

  • Ismail MA, Amin MA, Eid AM, Hassan SE, Mahgoub HAM, Lashin I, Abdelwahab AT, Azab E, Gobouri AA, Elkelish A, Fouda A (2021) Comparative Study between exogenously applied plant growth hormones versus metabolites of microbial endophytes as plant growth-promoting for Phaseolus vulgaris L. Cells 10:1059

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaemsaeng R, Jantasuriyarat C, Thamchaipenet A (2018) Molecular interaction of 1-aminocyclopropane-1-carboxylate deaminase (ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards salt-stress resistance of Oryza sativa L. cv. KDML105. Sci Rep 8:1950

    Article  PubMed  PubMed Central  Google Scholar 

  • Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458

    Article  Google Scholar 

  • Jasim B, John Jimtha C, Jyothis M, Radhakrishnan EK (2013) Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul 71:1–11

    Article  CAS  Google Scholar 

  • Joe MM, Devaraj S, Benson A, Sa T (2016) Isolation of phosphate solubilizing endophytic bacteria from Phyllanthus amarus Schum & Thonn: Evaluation of plant growth promotion and antioxidant activity under salt stress. J Appl Res Med Aromatic Plants 3:71–77

    Article  Google Scholar 

  • Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agron 2019:1–7. https://doi.org/10.1155/2019/4917256

    Article  CAS  Google Scholar 

  • Kannan R, Damodaran T, Umamaheswari S (2015) Sodicity tolerant polyembryonic mango root stock plants: a putative role of endophytic bacteria. Afr J Biotech 14:350–359

    Article  Google Scholar 

  • Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasote DM, Katyare SS, Hegde MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci 11:982–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khalil AMA, Hassan SE, Alsharif SM, Eid AM, Ewais EE, Azab E, Gobouri AA, Elkelish A, Fouda A (2021) Isolation and characterization of fungal endophytes isolated from medicinal plant Ephedra pachyclada as plant growth-promoting. Biomolecules 11:140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AL, Al-Harrasi A, Al-Rawahi A, Al-Farsi Z, Al-Mamari A, Waqas M, Asaf S, Elyassi A, Mabood F, Shin J-H (2016) Endophytic fungi from Frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS ONE 11:e0158207

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MA, Asaf S, Khan AL, Ullah I, Ali S, Kang S-M, Lee I-J (2019) Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1. Ann Microbiol 69:797–808

    Article  CAS  Google Scholar 

  • Kumar A, Kumar A, Patel H (2018) Role of microbes in phosphorus availability and acquisition by plants. Int J Curr Microbiol App Sci 7:1344–1347

    Article  Google Scholar 

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

    Google Scholar 

  • Landa BB, Hervás A, Bettiol W, Jiménez-Díaz RM (1997) Antagonistic activity of Bacteria from the chickpea rhizosphere against Fusarium Oxysporum f. sp Ciceris. Phytoparasitica 25:305–318

    Article  Google Scholar 

  • Lane D (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. pp 115–175

  • Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276

    Article  CAS  PubMed  Google Scholar 

  • Leite MCBS, Farias ARBD, Freire FJ, Andreote FD, Kuklinsky-Sobral J, Freire MBGS (2014) Isolation, bioprospecting and diversity of salt-tolerant bacteria associated with sugarcane in soils of Pernambuco, Brazil. Revista Brasileira De Engenharia Agrícola e Ambiental 18:73–79

    Article  Google Scholar 

  • Lin Q-M, Rao Z-H, Sun Y-X, Yao J, Xing L-J (2002) Identification and practical application of silicate-dissolving bacteria. Agric Sci China 1:81–85

    Google Scholar 

  • Lin L, Li Z, Hu C, Zhang X, Chang S, Yang L, Li Y, An Q (2009) Plant growth-promoting nitrogen-fixing enterobacteria are in association with sugarcane plants growing in Guangxi, China. Microbes Environ 1204160379–1204160379

  • Maxton A, Singh P, Masih SA (2018) ACC deaminase-producing bacteria mediated drought and salt tolerance in Capsicum annuum. J Plant Nutr 41:574–583

    Article  CAS  Google Scholar 

  • Mbarki S, Cerdà A, Brestic M, Mahendra R, Abdelly C, Pascual JA (2017) Vineyard compost supplemented with Trichoderma Harzianum T78 improve saline soil quality. Land Degrad Dev 28:1028–1037

    Article  Google Scholar 

  • Mei L, Zhu M, Zhang D-Z, Wang Y-Z, Guo J, Zhang H-B (2014) Geographical and temporal changes of foliar fungal endophytes associated with the invasive plant Ageratina adenophora. Microb Ecol 67:402–409

    Article  PubMed  Google Scholar 

  • Miller D, Bryant J, Madsen E, Ghiorse W (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MiloÅ¡ević NA, Marinković JB, Tintor BB (2012) Mitigating abiotic stress in crop plants by microorganisms. Zbornik Matice Srpske Za Prirodne Nauke. https://doi.org/10.2298/ZMSPN1223017M

    Article  Google Scholar 

  • Mishra IG, Sharma A (2012) Exogenously supplied osmoprotectants confer enhanced salinity tolerance in rhizobacteria. J Ecobiotechnol

  • Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mutlu S, Atici Ö, Nalbantoglu B (2009) Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. Biol Plant 53:334–338

    Article  CAS  Google Scholar 

  • Nabti E, Schmid M, Hartmann A (2015) Application of halotolerant bacteria to restore plant growth under salt stress. Halophiles. Springer, pp 235–259

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • 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 209:21–32

    Article  CAS  PubMed  Google Scholar 

  • Otieno N, Lally R, Kiwanuka S, Lloyd A, Ryan D, Germaine K, Dowling D (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00745

    Article  Google Scholar 

  • Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Appl Microbiol 117:766–773

    Article  CAS  PubMed  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 

  • Paul D, Sinha SN (2015) Isolation and characterization of a phosphate solubilizing heavy metal tolerant bacterium from River Ganga, West Bengal, India. Songklanakarin J Sci Technol 37:651–657

    CAS  Google Scholar 

  • Pimentel D, Berger B, Filiberto D, Newton M, Wolfe B, Karabinakis E, Clark S, Poon E, Abbett E, Nandagopal S (2004) Water resources: agricultural and environmental issues. Bioscience 54:909–918

    Article  Google Scholar 

  • Pinedo I, Ledger T, Greve M, Poupin MJ (2015) Burkholderia phytofirmans PsJN induces long-term metabolic and transcriptional changes involved in Arabidopsis thaliana salt tolerance. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00466

    Article  PubMed  PubMed Central  Google Scholar 

  • Pirhadi M, Enayatizamir N, Motamedi H, Sorkheh K (2016) Screening of salt tolerant sugarcane endophytic bacteria with potassium and zinc for their solubilizing and antifungal activity. Biosci Biotech Res Comm 9:530–538

    Article  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 Fertil Soils 52:119–125

    Article  CAS  Google Scholar 

  • Rabie G, Almadini A (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotech 4:210–222

    CAS  Google Scholar 

  • Rodrigues AA, Forzani MV, Soares RDS, Sibov ST, Vieira JDG (2016) Isolation and selection of plant growth-promoting bacteria associated with sugarcane. Pesquisa Agropecuária Tropical 46:149–158

    Article  Google Scholar 

  • Sairam R, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 407–421

  • Salisbury F, Ross C (1998) Plant physiology. Wads Worth Pub Co, Belmont

    Google Scholar 

  • Sandhya V, Sk ZA, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26

    Article  CAS  Google Scholar 

  • Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Saravanakumar D, Kavino M, Raguchander T, Subbian P, Samiyappan R (2011) Plant growth promoting bacteria enhance water stress resistance in green gram plants. Acta Physiol Plant 33:203–209

    Article  CAS  Google Scholar 

  • Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biol Med 30:1191–1212

    Article  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92

    Article  PubMed  PubMed Central  Google Scholar 

  • Selvi K, Paul J, Vijaya V, Saraswathi K (2017) Analyzing the efficacy of phosphate solubilizing microorganisms by enrichment culture techniques. Biochem Mol Biol J 3:1–7

    Google Scholar 

  • Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Article  CAS  PubMed  Google Scholar 

  • Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (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 

  • Shahid M, Akram MS, Khan MA, Zubair M, Shah SM, Ismail M, Shabir G, Basheer S, Aslam K, Tariq M (2018) A phytobeneficial strain Planomicrobium sp. MSSA-10 triggered oxidative stress responsive mechanisms and regulated the growth of pea plants under induced saline environment. J Appl Microbiol 124:1566–1579

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01600

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheng X-F, He L-Y, Huang W-Y (2002) The conditions of releasing potassium by a silicate-dissolving bacterial strain NBT. Agric Sci China 1:662–666

    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 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. https://doi.org/10.3389/fpls.2016.01890

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh P, Kumar V, Agrawal S (2014) Evaluation of phytase producing bacteria for their plant growth promoting activities. Int J Microbiol 2014

  • Sivritepe N, Sivritepe HO, Eris A (2003) The effects of NaCl priming on salt tolerance in melon seedlings grown under saline conditions. Sci Hortic 97:229–237

    Article  CAS  Google Scholar 

  • SkÅ‚odowska M, GapiÅ„ska M, Gajewska E, Gabara B (2009) Tocopherol content and enzymatic antioxidant activities in chloroplasts from NaCl-stressed tomato plants. Acta Physiol Plant 31:393–400

    Article  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314

    Article  CAS  PubMed  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 

  • Takahashi R, Nishio T, Ichizen N, Takano T (2007) High-affinity K+ transporter PhaHAK5 is expressed only in salt-sensitive reed plants and shows Na+ permeability under NaCl stress. Plant Cell Rep 26:1673–1679

    Article  CAS  PubMed  Google Scholar 

  • Tewari S, Arora NK (2016) Fluorescent Pseudomonas sp. PF17 as an efficient plant growth regulator and biocontrol agent for sunflower crop under saline conditions. Symbiosis 68:99–108

    Article  CAS  Google Scholar 

  • Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem PPB 99:108–117

    Article  CAS  PubMed  Google Scholar 

  • Ullah I, Khan AR, Park G-S, Lim J-H, Waqas M, Lee I-J, Shin J-H (2013) Analysis of phytohormones and phosphate solubilization in Photorhabdus spp. Food Sci Biotechnol 22:25–31

    Article  CAS  Google Scholar 

  • Vaishnav A, Choudhary DK (2019) Regulation of drought-responsive gene expression in Glycine max L. Merrill is mediated through Pseudomonas simiae strain AU. J Plant Growth Regul 38:333–342

    Article  CAS  Google Scholar 

  • Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growth-promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance. Antonie Van Leeuwenhoek 107:1519–1532

    Article  CAS  PubMed  Google Scholar 

  • Younesi O, Moradi A (2014) Effects of plant growth-promoting rhizobacterium (PGPR) and arbuscular mycorrhizal fungus (AMF) on antioxidant enzyme activities in salt-stressed bean (Phaseolus vulgaris L.). Agriculture (pol’nohospodárstvo) 60:10–21

    Article  CAS  Google Scholar 

  • Zaferanloo B, Virkar A, Mahon PJ, Palombo EA (2013) Endophytes from an Australian native plant are a promising source of industrially useful enzymes. World J Microbiol Biotechnol 29:335–345

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Xu Y, Lai X (2018) Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Braz J Microbiol 49:269–278

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was not supported by any funding.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by [HAMM], [AF], [AME], [EE-DE], and [SE-DH]. The first draft of the manuscript was written by [HAMM], [AF], [AME], and [SE-DH], and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Amr Fouda.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 154 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahgoub, H.A.M., Fouda, A., Eid, A.M. et al. Biotechnological application of plant growth-promoting endophytic bacteria isolated from halophytic plants to ameliorate salinity tolerance of Vicia faba L.. Plant Biotechnol Rep 15, 819–843 (2021). https://doi.org/10.1007/s11816-021-00716-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-021-00716-y

Keywords

Navigation