Abstract
Some plant growth-promoting bacteria (PGPR) can ameliorate abiotic stressors like drought stress and promote plant growth. The present study investigated various drought-tolerant mechanisms of Enterobacter bugandensis WRS7, a rhizospheric isolate, by which it alleviates the deleterious effects of drought stress in wheat plants (Triticum aestivum L). The isolate WRS7 showed different plant growth-promoting properties, including nitrogen fixation, phosphate solubilization, siderophore production, phytohormone (indole acetic acid and gibberellic acid) production, exopolysaccharide secretion, and ACC deaminase activity. Its inoculation to wheat plants improved plant growth in terms of root/shoot growth and chlorophyll content. Its inoculation also exhibited drought stress ameliorating properties, including increased osmolyte content (proline and total soluble sugar), relative water content, catalase and superoxide dismutase activity, and decreased lipid peroxidation compared to non-inoculated plants. Our biochemical data were coherent with gene expression analysis of WRS7-treated plants, which showed altered expression of genes encoding antioxidant enzymes (CAT, APX, and GPX), osmolyte synthesis (P5CS, P5CR, and TPS1), biosynthesis of stress hormone genes (NCED, WZE, SAMS, ACS1, and ACO encoding proteins for the biosynthesis of abscisic acid and ethylene), and calcium transporter (TPC1) in the wheat plant. The regulation of the ethylene biosynthesis gene and modulation of TPC1 gene expression by PGPR E. bugandensis WRS7 in wheat plants highlights its additional role in alleviating drought stress. The colonization study demonstrated the successful colonization of E. bugandensis WRS7 in wheat plants. Overall, the present study indicates that E. bugandensis WRS7 alleviates drought stress in wheat plants by differentially regulating various metabolic genes in treated plants.
Similar content being viewed by others
References
Abd El-Daim IA, Bejai S, Meijer J (2019) Bacillus velezensis 5113 induced metabolic and molecular reprogramming during abiotic stress tolerance in wheat. Sci Rep 9:16282
Abeles F, Morgan P, Saltveit M (1992) Ethylene in plant biology. Academic press, Cambridge
Aebi H (1984) [13] Catalase in vitro. Methods in enzymology. Elsevier, Amsterdam, pp 121–126
Ansari F, Jabeen M, Ahmad I (2021) Pseudomonas azotoformans FAP5, a novel biofilm-forming PGPR strain, alleviates drought stress in wheat plant. Int J Environ Sci Te 18:3855–3870
Aslam MM, Farhat F, Siddiqui MA, Yasmeen S, Khan MT, Sial MA, Khan IA (2021) Exploration of physiological and biochemical processes of canola with exogenously applied fertilizers and plant growth regulators under drought stress. PLoS ONE 16:e0260960
Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth-stimulation. Soil Biol Biochem 19:451–457
Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A (2017) Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 161:502–514
Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Battaglia M, Covarrubias AA (2013) Late embryogenesis abundant (LEA) proteins in legumes. Front Plant Sci 4:190
Bhatt RM, Selvakumar G, Upreti KK, Boregowda PC (2015) Effect of biopriming with Enterobacter strains on seed germination and seedling growth of tomato (Solanum lycopersicum L.) under osmotic stress. Proc Natl Acad Sci, India Sect. b: Biol Sci 85:63–69
Blatt MR (2000) Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Bio 16:221–241
Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503
Busse MD, Bottomley PJ (1989) Growth and nodulation responses of Rhizobium meliloti to water stress induced by permeating and nonpermeating solutes. Appl Environ Microbiol 55:2431–2436
Caverzan A, Casassola A, Brammer SP (2016) Antioxidant responses of wheat plants under stress. Genet Mol Biol 39:1–6
Chandra P, Wunnava A, Verma P, Chandra A, Sharma RK (2021) Strategies to mitigate the adverse effect of drought stress on crop plants—influences of soil bacteria: a review. Pedosphere 31:496–509
Chen L, Liu Y, Wu G, VeronicanNjeri K, Shen Q, Zhang N, Zhang R (2016) Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol Plant 158:34–44
Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci 111:6497–6502
Clarke D, Hess TM, Haro-Monteagudo D, Semenov M, Knox JW (2021) Assessing future drought risks and wheat yield losses in England. Agric Meteorol 297:108248
Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153:79–90
Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165
Dudziak K, Zapalska M, Börner A, Szczerba H, Kowalczyk K, Nowak M (2019) Analysis of wheat gene expression related to the oxidative stress response and signal transduction under short-term osmotic stress. Sci Rep 9:2743
Duxbury AC, Yentsch CS (1956) Plankton pigment nomographs. J Mar Res 15(1). https://elischolar.library.yale.edu/journal_of_marine_research/866
Dye D (1962) The inadequacy of the usual determinative tests for the identification of Xanthomonas spp. N Z J Sci 5:393–416
Egamberdieva D, Wirth S, Bellingrath-Kimura SD, Mishra J, Arora NK (2019) Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02791
Estrada-Melo AC, Chao C, Reid MS, Jiang C-Z (2015) Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Hortic Res 2:15013
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01147
FAO (2017) The future of food and agriculture—Trends and challenges. Rome
Fernandez O, Vandesteene L, Feil R, Baillieul F, Lunn JE, Clément C (2012) Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance. Planta 236:355–369
Ghosh R, Barman S, Mukherjee R, Mandal NC (2016) Role of phosphate solubilizing Burkholderia spp. for successful colonization and growth promotion of Lycopodium cernuum L. (Lycopodiaceae) in lateritic belt of Birbhum district of West Bengal. India Microbiol Res 183:80–91
Ghosh D, Sen S, Mohapatra S (2017) Modulation of proline metabolic gene expression in Arabidopsis thaliana under water-stressed conditions by a drought-mitigating Pseudomonas putida strain. Annals Microbiol 67:655–668
Ghosh D, Gupta A, Mohapatra S (2019) A comparative analysis of exopolysaccharide and phytohormone secretions by four drought-tolerant rhizobacterial strains and their impact on osmotic-stress mitigation in Arabidopsis thaliana. World J Microbiol Biotechnol 35:1–15
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318
Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Amelioration of drought tolerance in wheat by the interaction of plant growth-promoting rhizobacteria. Plant Biol 18:992–1000
Gontia-Mishra I, Sapre S, Kachare S, Tiwari S (2017) Molecular diversity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing PGPR from wheat (Triticum aestivum L.) rhizosphere. Plant Soil 414:213–227
Górka B, Wieczorek PP (2017) Simultaneous determination of nine phytohormones in seaweed and algae extracts by HPLC-PDA. J Chromatogr B 1057:32–39
Gowtham H, Singh B, Murali M, Shilpa N, Prasad M, Aiyaz M, Amruthesh K, Niranjana S (2020) Induction of drought tolerance in tomato upon the application of ACC deaminase producing plant growth promoting rhizobacterium Bacillus subtilis Rhizo SF 48. Microbiol Res 234:126422
Gupta G, Panwar J, Jha PN (2013) Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br Appl Soil Ecol 64:252–261
Gupta S, Seth R, Sharma A (2016) Plant growth-promoting rhizobacteria play a role as phytostimulators for sustainable agriculture. Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 475–493
Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran L-SP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420
Irigoyen J, Einerich D, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 84:55–60
Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487
Keswani C, Prakash O, Bharti N, Vílchez JI, Sansinenea E, Lally RD, Borriss R, Singh SP, Gupta VK, Fraceto LF (2019) Re-addressing the biosafety issues of plant growth promoting rhizobacteria. Sci Total Environ 690:841–852
Khan N, Bano A (2019) Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 14:e0222302
Kohler J, Hernández JA, Caravaca F, Roldán A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151
Kosová K, Holková L, Prášil IT, Prášilová P, Bradáčová M, Vítámvás P, Čapková V (2008) Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare). J Plant Physiol 165:1142–1151
Larisch N, Kirsch SA, Schambony A, Studtrucker T, Böckmann RA, Dietrich P (2016) The function of the two-pore channel TPC1 depends on dimerization of its carboxy-terminal helix. Cell Mol Life Sci 73:2565–2581
Li W, Raoult D, Fournier P-E (2009) Bacterial strain typing in the genomic era. FEMS Microbiol Rev 33:892–916
Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336
Liu J, Niu Y, Zhang J, Zhou Y, Ma Z, Huang X (2018) Ca2+ channels and Ca2+ signals involved in abiotic stress responses in plant cells: recent advances. Plant Cell Tiss Organ Cult (PCTOC) 132:413–424
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Martins SJ, Rocha GA, de Melo HC, de Castro GR, Ulhôa CJ, de Campos DÉ, Oshiquiri LH, da Cunha MG, da Rocha MR, de Araújo LG (2018) Plant-associated bacteria mitigate drought stress in soybean. Environ Sci Pollut Res 25:13676–13686
Mehrabad Pour-Benab S, Fabriki-Ourang S, Mehrabi A-A (2019) Expression of dehydrin and antioxidant genes and enzymatic antioxidant defense under drought stress in wild relatives of wheat. Biotechnol Biotechnol Equip 33:1063–1073
Murali M, Singh SB, Gowtham H, Shilpa N, Prasad M, Aiyaz M, Amruthesh K (2021) Induction of drought tolerance in Pennisetum glaucum by ACC deaminase producing PGPR-Bacillus amyloliquefaciens through antioxidant defense system. Microbiol Res 253:126891
Niu X, Song L, Xiao Y, Ge W (2018) Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front Microbiol 8:2580
Noman A, Ali Q, Maqsood J, Iqbal N, Javed MT, Rasool N, Naseem J (2018) Deciphering physio-biochemical, yield, and nutritional quality attributes of water-stressed radish (Raphanus sativus L.) plants grown from Zn-Lys primed seeds. Chemosphere 195:175–189
Pandey GK, Sanyal SK (2021) Plant ion channels without molecular identity and two-pore channel 1. Functional dissection of calcium homeostasis and transport machinery in plants. Springer International Publishing, Cham, pp 43–52
Pati NB, Doijad SP, Schultze T, Mannala GK, Yao Y, Jaiswal S, Ryan D, Suar M, Gwozdzinski K, Bunk B, Mraheil MA, Marahiel MA, Hegemann JD, Spröer C, Goesmann A, Falgenhauer L, Hain T, Imirzalioglu C, Mshana SE, Overmann J, Chakraborty T (2018) Enterobacter bugandensis: a novel enterobacterial species associated with severe clinical infection. Sci Rep 8(1):5392
Prescott LM, Harley JP (2002) Harley prescott: laboratory exercises in microbiology, 5th edn. McGraw-Hill, New York
Ramirez D, Giron M (2022) Enterobacter Infections (Jan 2023). [Updated 2022 Jun 27]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available from https://www.ncbi.nlm.nih.gov/books/NBK559296/
Rashid U, Yasmin H, Hassan MN, Naz R, Nosheen A, Sajjad M, Ilyas N, Keyani R, Jabeen Z, Mumtaz S (2021) Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep 41:549–569
Reinhold-Hurek B, Hurek T, Claeyssens M, Van Montagu M (1993) Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root-invading diazotroph. J Bacteriol 175:7056–7065
Sadak MS (2019) Physiological role of trehalose on enhancing salinity tolerance of wheat plant. Bull Natl Res Cent 43:1–10
Sarma RK, Saikia R (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377:111–126
Simons M, Van Der Bij A, Brand I, De Weger L, Wijffelman C, Lugtenberg B (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant-Microbe Interact: MPMI 9:600–607
Singh RP, Jha P, Jha PN (2015a) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 184:57–67
Singh RP, Shelke GM, Kumar A, Jha PN (2015b) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:937
Singh RP, Runthala A, Khan S, Jha PN (2017) Quantitative proteomics analysis reveals the tolerance of wheat to salt stress in response to Enterobacter cloacae SBP-8. PLoS ONE 12:e0183513
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
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
Vaishnav A, Singh J, Singh P, Rajput RS, Singh HB, Sarma BK (2020) Sphingobacterium sp BHU-AV3 induces salt tolerance in tomato by enhancing antioxidant activities and energy metabolism. Front Microbiol 11:443
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151
Wang Y-J, Yu J-N, Chen T, Zhang Z-G, Hao Y-J, Zhang J-S, Chen S-Y (2005) Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. J Exp Bot 56:3051–3060
Wang X, Li Q, Xie J, Huang M, Cai J, Zhou Q, Dai T, Jiang D (2021) Abscisic acid and jasmonic acid are involved in drought priming-induced tolerance to drought in wheat. Crop J 9:120–132
White EJ, Venter M, Hiten NF, Burger JT (2008) Modified Cetyltrimethylammonium bromide method improves robustness and versatility: the benchmark for plant RNA extraction. Wiley Online Library, New York
Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183
Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608
Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agric Res 56:715–721
Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Acknowledgements
SA is thankful to DST-INSPIRE, government of India, for providing a research fellowship. We acknowledge Department of Biological Sciences, BITS Pilani, Pilani campus for logistic support, Sophisticated Instrument Facility, BITS Pilani, Pilani for FESEM facility, and Indian Institute of Wheat and Barley Research, Karnal for providing wheat variety WH1142. We would like to thank Department of Chemistry, BITS Pilani for HRMS facility.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. PJ has supervised the theme of work. All experiments were performed by SA. The first draft of the manuscript was written by SA. PJ wrote and edited the manuscript. Both authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
We declare that we have no conflicts of interest related to this work; this paper has not been published previously.
Additional information
Handling Editor: Chetan Keswani.
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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Arora, S., Jha, P.N. Drought-Tolerant Enterobacter bugandensis WRS7 Induces Systemic Tolerance in Triticum aestivum L. (Wheat) Under Drought Conditions. J Plant Growth Regul 42, 7715–7730 (2023). https://doi.org/10.1007/s00344-023-11044-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11044-6