Skip to main content

Advertisement

Log in

Drought tolerance improvement in plants: an endophytic bacterial approach

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Climate change is a crucial issue among the serious emerging problems which got a global attention in the last few decades. With the climate change, worldwide crop production has been seriously affected by drought stress. In this regard, various technologies including traditional breeding and genetic engineering are used to cope with drought stress. However, the interactions between plants and endophytic bacteria emerged as an interesting era of knowledge that can be used for novel agriculture practices. Endophytic bacteria which survive within plant tissues are among the most appropriate technologies improving plant growth and yield under drought conditions. These endophytic bacteria live within plant tissues and release various phytochemicals that assist plant to withstand in harsh environmental conditions, i.e., drought stress. Their plant growth–promoting characteristics include nitrogen fixation, phosphate solubilization, mineral uptake, and the production of siderophore, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, and various phytohormones. These plant growth promoting characteristics of endophytic bacteria improve root length and density, which lead to the enhance drought tolerance. In addition, plant–endophytic bacteria assist plant to withstand against drought stress by producing drought-tolerant substances, for instance, abscisic acid, indole-3-acetic acid, ACC deaminase, and various volatile compounds. Indirectly, endophytic bacteria also improve osmotic adjustment, relative water content, and antioxidant activity of inoculated plants. Altogether, these bacterial-mediated drought tolerance and plant growth–promoting processes continue even under severe drought conditions which lead to enhanced plant growth promotion and yield. The present review highlights a natural and environment-friendly strategy in the form of drought-tolerant and plant growth–promoting endophytic bacteria to improve drought tolerance in plants.

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

Similar content being viewed by others

References

  • Ali S, Kim WC (2018) Plant growth promotion under water: decrease of waterlogging-induced ACC and ethylene levels by ACC deaminase-producing bacteria. Front Microbiol 9:1096

    Article  PubMed  PubMed Central  Google Scholar 

  • Asaf S, Khan AL, Khan MA, Imran QM, Yun BW, Lee IJ (2017) Osmoprotective functions conferred to soybean plants via inoculation with Sphingomonas sp LK11 and exogenous trehalose. Microbiol Res 205:135–145

    Article  CAS  PubMed  Google Scholar 

  • Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants-role of plant growth regulators. Protoplasma 252:399–413

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M (2010) Inducing drought tolerance in plants: some recent advances. Biotechnol Adv 28:169–183

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Attia M, Ahmed M, El-Sonbaty M (2009) Use of biotechnologies to increase growth, productivity and fruit quality of Maghrabi banana under different rates of phosphorus. World J Agric Sci 5:211–220

    CAS  Google Scholar 

  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol 181:413–423

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Hallmann J (2006) Control of plant pathogenic fungi with bacterial endophytes. In Microbial root endophytes. Springer pp 53-69.

  • Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Factories 13:66

    Article  Google Scholar 

  • Bhore SJ, Ravichantar N, 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 

  • Bielach A, Hrtyan M, Tognetti VB (2017) Plants under stress: involvement of auxin and cytokinin. Int J Mol Sci 18:1427

    Article  CAS  PubMed Central  Google Scholar 

  • Budak H, Kantar M, Yucebilgili Kurtoglu K (2013) Drought tolerance in modern and wild wheat. Sci World J 2016(548246):16

    Google Scholar 

  • Cardoso P, Alves A, Silveira P, Sá C, Fidalgo C, Freitas R, Figueira E (2018) Bacteria from nodules of wild legume species: phylogenetic diversity, plant growth promotion abilities and osmotolerance. Sci Total Environ 645:1094–1102

    Article  CAS  PubMed  Google Scholar 

  • Carmen CA, Patricia P, Rubén B, Victoria SM (2016) Plant–rhizobacteria interaction and drought stress tolerance in plants in drought stress tolerance in plants. Springer, Cham, pp 287–308

    Google Scholar 

  • Cassán F, Vanderleyden J, Spaepen S (2013) Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. Plant Biol 35:1–20

    Google Scholar 

  • Chapman N, Miller AJ, Lindsey K, Whalley WR (2012) Roots, water, and nutrient acquisition: let’s get physical. Trends Plant Sci 17:701–710

    Article  CAS  PubMed  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7:41564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Rekha P, Arun A, Shen F, Lai WA, Young C (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Bot 87:455–462

    Article  CAS  Google Scholar 

  • Comas L, Becker S, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005a) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005b) Endophytic colonization of Vitis vinifera L by plant growth-promoting bacterium Burkholderia sp strain PsJN. Appl Environ Microbiol 71:1685–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper M, Gho C, Leafgren R, Tang T, Messina C (2014) Breeding drought tolerant maize hybrids for the US corn-belt: discovery to product. J Exp Bot 65:6191–6204

    Article  CAS  PubMed  Google Scholar 

  • Daryanto S, Wang L, Jacinthe PA (2016) Global synthesis of drought effects on maize and wheat production. PLoS One 11:e0156362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dekas AE, Poretsky RS, Orphan VJ (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326:422–426

    Article  CAS  PubMed  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48

    Article  PubMed  Google Scholar 

  • Egamberdieva D, Wirth SJ, Alqarawi AA, Abd Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. FMC 8:2104

    Google Scholar 

  • Eisenstein M (2013) Discovery in a dry spell. Nature 501:S7–S9

    Article  CAS  PubMed  Google Scholar 

  • Etminani F, Harighi B (2018) Isolation and identification of endophytic bacteria with plant growth promoting activity and biocontrol potential from wild pistachio. Trees Plant Pathol J 34:208–217

    CAS  PubMed  Google Scholar 

  • Fedoroff NV, Battisti DS, Beachy RN, Cooper PJM, Fischhoff DA, Hodges CN, Zhu JK (2010) Radically rethinking agriculture for the 21st century. Science 327:833–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel OM, Castrillo G, Paredes SH, González IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163

    Article  PubMed  PubMed Central  Google Scholar 

  • Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L) isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152

    Article  CAS  PubMed  Google Scholar 

  • Gagne-Bourgue F, Aliferis KA, Seguin P, Rani M, Samson R, Jabaji S (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switch grass (Panicum virgatum L) cultivars. J Appl Microbiol 114:836–853

    Article  CAS  PubMed  Google Scholar 

  • Gagné-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 

  • Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169:13–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Govindasamy V, George P, Raina SK, Kumar M, Rane J, Annapurna K (2018) Plant-associated microbial interactions in the soil environment: role of endophytes in imparting abiotic stress tolerance to crops. In: Advances in Crop Environment Interaction. Springer, Singapore, pp 245–284

    Chapter  Google Scholar 

  • Gregory PJ (2008) Plant roots: growth, activity and interactions with the soil. John Wiley & Sons pp 23-34.

  • Guajardo E, Correa JA, Contreras-Porcia L (2016) Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243:767–781

    Article  CAS  PubMed  Google Scholar 

  • Gunnell D, Eddleston M, Phillips MR, Konradsen F (2007) The global distribution of fatal pesticide self-poisoning: systematic review. BMC Public Health 7:357

    Article  PubMed  PubMed Central  Google Scholar 

  • Hallmann J (2001) Plant interactions with endophytic bacteria CABI Publishing. New York pp:87–119

  • Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. In Microbial root endophytes Springer, Berlin, Heidelberg, pp 15-31.

  • Halo BA, Khan AL, Waqas M, AlHarrasi A, Hussain J, Ali L, Adnan M, Lee IJ (2015) Endophytic bacteria (Sphingomonas sp LK11) and gibberellin can improve Solanum lycopersicum growth and oxidative stress under salinity. J Plant Interact 10:117–125

    Article  CAS  Google Scholar 

  • Hameeda B, Harini G, Rupela O, Wani S, Reddy G (2008) Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. Microbiol Res 163:234–242

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (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 

  • Hardoim PR, van Overbeek LS, Elsas JDV (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, Schmid M, Van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Hayashi KI (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53:965–975

    Article  CAS  PubMed  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. J Agric Food Chem 42:1825–1831

    CAS  Google Scholar 

  • Huang B, DaCosta M, Jiang Y (2014) Research advances in mechanisms of turf grass tolerance to abiotic stresses: from physiology to molecular biology. Crit Rev Plant Sci 33:141–189

    Article  CAS  Google Scholar 

  • Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant-Microbe Interact 17:1078–1085

    Article  CAS  PubMed  Google Scholar 

  • Jiao J, Ma Y, Chen S, Liu C, Song Y, Qin Y, Liu Y (2016) Melatonin-producing endophytic bacteria from grapevine roots promote the abiotic stress-induced production of endogenous melatonin in their hosts. Front Plant Sci 7:1387

    Article  PubMed  PubMed Central  Google Scholar 

  • Johansen KS (2016) Lytic polysaccharide monooxygenases: the microbial power tool for lignocellulose degradation. Trends Plant Sci 21:926–936

    Article  CAS  PubMed  Google Scholar 

  • Jung H, Lee DK, Do Choi Y, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312

    Article  CAS  PubMed  Google Scholar 

  • Kandel S, Joubert P, Doty S (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77

    Article  CAS  PubMed Central  Google Scholar 

  • Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665

    Article  PubMed  PubMed Central  Google Scholar 

  • Khadri M, Tejera NA, Lluch C (2006) Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J Plant Growth Regul 25:110–119

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Khan Z, Rho H, Firrincieli A, Hung SH, Luna V, Masciarelli O, Doty SL (2016) Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Current Plant Biol 6:38–47

    Article  Google Scholar 

  • Kiani SP, Talia P, Maury P, Grieu P, Heinz R, Perrault A, Sarrafi A (2007) Genetic analysis of plant water status and osmotic adjustment in recombinant inbred lines of sunflower under two water treatments. Plant Sci 172:773–787

    Article  CAS  Google Scholar 

  • Koevoets IT, Venema JH, Elzenga JT, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1335

    Article  PubMed  PubMed Central  Google Scholar 

  • Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • Lee S, Flores-Encarnacion M, Contreras-Zentella M, Garcia-Flores L, Escamilla J, Kennedy C (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c biogenesis genes. J Bacteriol 186:5384–5391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lery L, von Krüger W, Viana F, Teixeira K, Bisch P (2008) A comparative proteomic analysis of Gluconacetobacter diazotrophicus PAL5 at exponential and stationary phases of cultures in the presence of high and low levels of inorganic nitrogen compound. Biochim Biophys Acta, Proteins Proteomics 1784:1578–1589

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Moreno A, Zhang C, Freitas H (2017) Serpentine endophytic bacterium Pseudomonas azotoformans ASS1 accelerates phytoremediation of soil metals under drought stress. Chemosphere 185:75–85

    Article  CAS  PubMed  Google Scholar 

  • Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM Fungi and Bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124

    Article  CAS  Google Scholar 

  • Mei C, Flinn BS (2010) The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Patents Biotech 4:81–95

    Article  CAS  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Mullan D, Pietragalla J (2012) Leaf relative water content Physiological breeding II: a field guide to wheat phenotyping CIMMYT, Mexico, 25-27.

  • Nascimento FX, Rossi MJ, Glick BR (2018) Ethylene and 1-aminocyclopropane-1-carboxylate (ACC) in plant–bacterial interactions. Front Plant Sci 9:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014a) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131

    Article  CAS  Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014b) 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 

  • Ngumbi E, Kloepper J (2016) Bacterial-mediated drought tolerance: current and future prospects. Appl Soil Ecol 105:109–125

    Article  Google Scholar 

  • Nounjan N, Chansongkrow P, Charoensawan V, Siangliw JL, Toojinda T, Chadchawan S, Theerakulpisut P (2018) High performance of photosynthesis and osmotic adjustment are associated with salt tolerance ability in rice carrying drought tolerance QTL: physiological and co-expression network analysis. Front Plant Sci 9:1135

    Article  PubMed  PubMed Central  Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olatunji D, Geelen D, Verstraeten I (2017) Control of endogenous auxin levels in plant root development. Int J Mol Sci 1812:2587

    Article  CAS  Google Scholar 

  • Oliveira A, Stoffels M, Schmid M, Reis V, Baldani J, Hartmann A (2009) Colonization of sugarcane plantlets by mixed inoculations with diazotrophic bacteria. Eur J Soil Biol 45:106–113

    Article  CAS  Google Scholar 

  • Pajares S, Bohannan BJ (2016) Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045

    PubMed  PubMed Central  Google Scholar 

  • Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752

    Article  Google Scholar 

  • Pedraza RO (2008) Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 125:25–35

    Article  CAS  PubMed  Google Scholar 

  • Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  CAS  PubMed  Google Scholar 

  • Pretty J, Bharucha ZP (2014) Sustainable intensification in agricultural systems. Ann Bot 114:1571–1596

    Article  PubMed  PubMed Central  Google Scholar 

  • Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IM, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–41

    Article  CAS  PubMed  Google Scholar 

  • Ravanbakhsh M, Sasidharan R, Voesenek L, Kowalchuk GA, Jousset A (2018) Microbial modulation of plant ethylene signaling: ecological and evolutionary consequences. Microbiome 6:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Reinhardt EL, Ramos PL, Manfio GP, Barbosa HR, Pavan C, Moreira-Filho CA (2008) Molecular characterization of nitrogen-fixing bacteria isolated from brazilian agricultural plants at São Paulo state Braz. J Microbiol 3:414–422

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19:827–837

    Article  CAS  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767

    Article  CAS  PubMed  PubMed Central  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 

  • Saravanan V, Madhaiyan M, Osborne J, Thangaraju M, Sa T (2008) Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microb Ecol 55:130–140

    Article  CAS  PubMed  Google Scholar 

  • Sarma RK, Saikia R (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377:111–126

    Article  CAS  Google Scholar 

  • Schwab F, Zhai G, Kern M, Turner A, Schnoor JL, Wiesner MR (2016) Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants–critical review. Nanotoxicology 10:257–278

    CAS  PubMed  Google Scholar 

  • Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Wang-Pruski G (2005) Burkholderia phytofirmans sp nov, a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192

    Article  CAS  PubMed  Google Scholar 

  • Shahzad R, Khan AL, Bilal S, Waqas M, Kang SM, Lee IJ (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 

  • Shakir MA, Asghari B, Arshad M (2012) Rhizosphere bacteria containing ACC deaminase conferred drought tolerance in wheat grown under semi-arid climate. Soil Environ 31:108–112

    CAS  Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:a001438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:130

    Article  PubMed  PubMed Central  Google Scholar 

  • Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ 36:909–919

    Article  CAS  PubMed  Google Scholar 

  • Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone. J Plant Res 124:437–453

    Article  CAS  PubMed  Google Scholar 

  • Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kannaste A, Behers L, Niinemets U (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9:e96086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson AC (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664

    Article  CAS  PubMed  Google Scholar 

  • Tuberosa R, Salvi S, Giuliani S, Sanguineti MC, Frascaroli E, Conti S, Landi P (2011) Genomics of root architecture and functions in maize In Root genomics. Springer, Berlin, Heidelberg, p 179204

    Google Scholar 

  • Ullah A, Akbar A, Luo Q, Khan AH, Manghwar H, Shaban M, Yang X (2019a) Microbiome diversity in cotton rhizosphere under normal and drought conditions. Microb Ecol 77:429–439

    Article  CAS  PubMed  Google Scholar 

  • Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015a) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40

    Article  CAS  Google Scholar 

  • Ullah A, Manghwar H, Shaban M, Khan AH, Akbar A, Ali U, Fahad S (2019b) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25:33103–33118

    Article  CAS  Google Scholar 

  • Ullah A, Mushtaq H, Ali H, Munis MFH, Javed MT, Chaudhary HJ (2015b) Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res 22:2505–2514

    Article  CAS  Google Scholar 

  • Ullah A, Mushtaq H, Fahad S, Shah A, Chaudhary HJ (2017b) Plant growth promoting potential of bacterial endophytes in novel association with Olea ferruginea and Withania coagulans. Microbiology 86:119–127

    Article  CAS  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2018) A novel cotton WRKY gene, GhWRKY6-like, improves salt tolerance by activating the ABA signaling pathway and scavenging of reactive oxygen species. Physiol Plant 162:439–454

    Article  CAS  PubMed  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2017a) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15:271–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vargas L, Santa Brígida AB, MotaFilho JP, de Carvalho TG, Rojas CA, Vaneechoutte D, Hemerly AS (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS One 9:e114744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varshney RK, Pazhamala L, Kashiwagi J, Gaur PM, Krishnamurthy L, Hoisington D (2011) Genomics and physiological approaches for root trait breeding to improve drought tolerance in chickpea (Cicerarietinum L) In Root genomics. Springer, Berlin, Heidelberg, pp 233–250

    Google Scholar 

  • Vigani G, Rolli E, Marasco R, Dell’Orto M, Michoud G, Soussi A, Daffonchio D (2018) Root bacterial endophytes confer drought resistance and enhance expression and activity of a vacuolar H+-pumping pyrophosphatase in pepper plants. Environ Microbiol. https://doi.org/10.1111/1462-292014272

  • Vysotskaya LB, Korobova AV, Veselov SY, Dodd IC, Kudoyarova GR (2009) ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat. Funct Plant Biol 36:66–72

    Article  CAS  Google Scholar 

  • Wang B, Seiler JR, Mei C (2016) A microbial endophyte enhanced growth of switchgrass under two drought cycles improving leaf level physiology and leaf development. Environ Exp Bot 122:100–108

    Article  Google Scholar 

  • Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SS, Rebetzke GJ, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63:3485–3498

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Chu Y, Zhang W, Lang D, Zhang X (2019) Bacillus pumilus alleviates drought stress and increases metabolite accumulation in Glycyrrhiza uralensis. Fisch. Environ Exp Bot 158:99–106

    Article  CAS  Google Scholar 

  • Yandigeri MS, Meena KK, Singh D, Malviya N, Singh DP, Solanki MK, Arora DK (2012) Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul 68:411–420

    Article  CAS  Google Scholar 

  • Yu LH, Wu SJ, Peng YS, Liu RN, Chen X, Zhao P, Xu P, Zhu B, Jiao GL, Pei Y (2016) Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnol J 14:72–84

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

We received funds from the Higher Education Commission of Pakistan (No: 21-2297/SRGP/R&D/HEC/2018) under Startup Research Grant Program. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Abid Ullah.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ullah, A., Nisar, M., Ali, H. et al. Drought tolerance improvement in plants: an endophytic bacterial approach. Appl Microbiol Biotechnol 103, 7385–7397 (2019). https://doi.org/10.1007/s00253-019-10045-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-10045-4

Keywords

Navigation