Skip to main content
Log in

Glyphosate induced toxicity to chickpea plants and stress alleviation by herbicide tolerant phosphate solubilizing Burkholderia cepacia PSBB1 carrying multifarious plant growth promoting activities

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

In this study, strain PSBB1 isolated from Vicia faba rhizosphere was identified as Burkholderia cepacia, by 16S rDNA sequence analysis and characterized. Strain PSBB1 tolerated glyphosate up to 3200 μg ml−1 and produced IAA (81.6 μg ml−1), ACC deaminase (69.3 mg−1 protein h−1), SA (39.3 μg ml−1) and 2,3-DHBA (26.6 μg ml−1), solubilized insoluble P (50.8 μg ml−1) and secreted 29.4 μg ml−1 exopolysaccharides, which decreased with increasing concentrations of glyphosate. Cell damage following glyphosate application was visible under SEM and CLSM. The phytotoxicity of glyphosate on chickpea was variable but significant. B. cepacia mitigated toxicity and enhanced the size, dry matter, symbiosis, seed attributes and nutritional contents of chickpea. Further, B. cepacia strain PSBB1 declined the levels of CAT, POD, APX and GPX and MDA contents at 4332 μg kg−1 soil glyphosate. Proline also increased under glyphosate stress but declined in B. cepacia inoculated plants. The ability to tolerate higher concentration of glyphosate, the capacity to secrete plant growth regulators even under herbicide stress and potential to reduce the level of proline and antioxidant enzymes makes B. cepacia as an interesting choice for enhancing chickpea production in soils contaminated even with herbicides.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adami MFF, Modolo AJE, Adami PF (2017) White clover tolerance to herbicides applied at different rates and phenological stages. Afr J Agric Res 12(28):2336–2341

    Article  Google Scholar 

  • Ahmed B, Dwivedi S, Abdin MZ, Azam A, Al-Shaeri M, Khan MS, Musarrat J (2017) Mitochondrial and chromosomal damage induced by oxidative stress in Zn2+ ions, ZnO-bulk and ZnO-NPs treated Allium cepa roots. Sci Rep 7:40685. https://doi.org/10.1038/srep40685

    Article  CAS  Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12(1):39–45

    Article  CAS  Google Scholar 

  • Alori ET, Dare MO, Babalola OO (2017) Microbial inoculants for soil quality and plant health. In: Sustainable agriculture reviews. Springer International Publishing, Berlin, pp 281–307

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Appl Environ Microbiol 55:1665–1669

    Google Scholar 

  • Arthee R, Marimuthu P (2017) Studies on endophytic Burkholderia sp. From sugarcane and its screening for plant growth promoting potential. J Exp Biol 5:2

    Google Scholar 

  • Atkin CL, Neilands JB, Phaff HJ (1970) Rhodotorulic acid from species of Leucosporidium, Rhodosporidium, Rhodotorula, Sporidiobolus, and Sporobolomyces, and a new alanine-containing ferrichrome from Cryptococcus melibiosum. J Bacteriol 103(3):722–733

    CAS  Google Scholar 

  • Azarmi F, Mozafari V, Dahaji PA, Hamidpour M (2016) Biochemical, physiological and antioxidant enzymatic activity responses of pistachio seedlings treated with plant growth promoting rhizobacteria and Zn to salinity stress. Acta Physiol Plant 38:121

    Article  Google Scholar 

  • 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(4):451–457

    Article  CAS  Google Scholar 

  • Bates LS, Woldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Bitew Y, Alemayehu M (2017) Review article impact of crop production inputs on soil health: a review. https://doi.org/10.3923/ajps.2017.109.131

  • Brick JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57(2):535–538

    Google Scholar 

  • Chehelpar N, Tohidi-Moghadam HR, Ghoushchi F (2016) Hexaconazole foliar application alleviates water deficit effects in common bean. Pes Agro Tropic 46(3):301–310

    Article  Google Scholar 

  • Curá JA, Franz DR, Filosofía JE, Balestrasse KB (2017) Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms 5(3):41

    Article  Google Scholar 

  • Curran WS (2016) Persistence of herbicides in soil. Crop Soils 49(5):16–21

    Article  Google Scholar 

  • Deinum EE, Kohlen W, Geurts R (2016) Quantitative modelling of legume root nodule primordium induction by a diffusive signal of epidermal origin that inhibits auxin efflux. BMC Plant Boil 16(1):254

    Article  Google Scholar 

  • del Gallo M, Ercole C, Matteucci F (2017) Plant–bacteria interaction at the microscope. In: Méndez-Vilas A (ed) Microscopy and imaging science: practical approaches to applied research and education, pp 312–317

  • Ditta A, Khalid A (2016) Bio-organo-phos: a sustainable approach for managing phosphorus deficiency in agricultural soils. In: Organic fertilizers-from basic concepts to applied outcomes. InTech, Rijeka, Croatia. https://doi.org/10.5772/62473

  • Dorjey S, Dolkar D, Sharma R (2017) Plant growth promoting rhizobacteria Pseudomonas: a review. Int J Curr Microbiol App Sci 6(7):1335–1344

    Article  Google Scholar 

  • Dworkin M, Foster J (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–601

    CAS  Google Scholar 

  • Dye DW (1962) The inadequacy of the usual determinative tests for the identification of Xanthomonas spp. New Zeal J Sci 5(4):393–416

    Google Scholar 

  • Fernández-López MG, Popoca-Ursino C, Sánchez-Salinas E, Tinoco-Valencia R, Folch-Mallol JL, Dantán-González E, Laura Ortiz-Hernández M (2017) Enhancing methyl parathion degradation by the immobilization of Burkholderia sp. isolated from agricultural soils. Microbiol Open 6(5). https://doi.org/10.1002/mbo3.507

  • Ghosh PK, Maiti TK (2016) Structure of extracellular polysaccharides (EPS) produced by rhizobia and their functions in legume–bacteria symbiosis: a review. Achiev Life Sci 10(2):136–143

    Article  Google Scholar 

  • Glick BR, Todorovic B, Czarny J, Cheng Z (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26(5–6):227–242

    Article  CAS  Google Scholar 

  • Gopal M, Dutta D, Jha SK, Kalra S, Bandyopadhyay S, Das SK (2011) Biodegradation of imidacloprid and metribuzin by Burkholderia cepacia strain CH9. Pestic Res J 23(1):36–40

    CAS  Google Scholar 

  • Gordon S, Weber RP (1951) The colorimetric estimation of IAA. Plant Physiol 26:192–195

    Article  CAS  Google Scholar 

  • Goud VV, Murade NB, Khakre MS (2013) Efficacy of imazethapyr and quizalofop-ethyl herbicides on growth and yield of chickpea. Bioscan 8(3):1015–1018

    CAS  Google Scholar 

  • Hammerschmidt R, Nuckles EM, Kuć J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol Plant Pathol 20(1):977–1082

    Google Scholar 

  • Han Y, Wang R, Yang Z, Zhan Y (2015) 1-aminocyclopropane 1- carboxylate deaminase from Pseudomonas stutzeri A 1501 facilitates the growth of rice in the presence of salts or heavy metals. J Microbiol Biotechnol 2:1119–1128

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Herman PL, Behrens M, Chakraborty S (2005) A three-component dicamba O-demethylase from Pseudomonas maltophilia, strain DI-6 gene isolation, characterization, and heterologous expression. J Biol Chem 280(26):24759–24767

    Article  CAS  Google Scholar 

  • Holmes A, Govan J, Goldstein R (1998) Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health. Emerg Infect Dis 4(2):221

    Article  CAS  Google Scholar 

  • Holt GJ, Krieg NR, Sneath PHA (1994) Gram negative aerobic/microaerophilic rods and cocci. In: Bergey’s manual of determinative bacteriology, 9th edn. Williams and Wilkins, Lippincott, Philadelphia

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane 1-carboxylate deaminase. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Hossain MA, Hoque MA, Burritt DJ (2014) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Oxidative damage to plants. Elsevier, San Diego, pp 477–522

  • Iswaran V, Marwah TS (1980) A modified rapid Kjeldahl method for determination of total nitrogen in agricultural and biological materials. Geobios 7(6):281–282

    Google Scholar 

  • Jackson ML (1976) Soil chemical analysis. Prentice Hall, New Delhi

    Google Scholar 

  • Karishma B, Prasad SH (2016) Isolation, characterization and growth studies of malathion insecticide degrading bacteria. Int J Environ Sci 6(5):697–706

    CAS  Google Scholar 

  • Kaul S, Sharma SS, Mehta IK (2008) Free radical scavenging potential of l-proline: evidence from in vitro assays. Amino Acids 34(2):315–320

    Article  CAS  Google Scholar 

  • Kaushal M, Wani SP (2016) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66(1):35–42

    Article  CAS  Google Scholar 

  • Khalid S, Khokhar SN (2013) Interaction of herbicides and bio-inoculants with agricultural crops and weeds. Pak J Agric Res 26(4):299–308

    Google Scholar 

  • King JE (1932) The colorimetric determination of phosphorus. Biochem J 26:292–297

    Article  CAS  Google Scholar 

  • Kurth C, Kage H, Nett M (2016) Siderophores as molecular tools in medical and environmental applications. Org Biomol Chem 14(35):8212–8227

    Article  CAS  Google Scholar 

  • Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 37:1921–1942

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL (1951) Protein measurement with the Folin phenol reagent. J Boil Chem 193(1):265–275

    CAS  Google Scholar 

  • Madariaga-Navarrete A, Rodríguez-Pastrana BR, Villagómez-Ibarra JR (2017) Bioremediation model for atrazine contaminated agricultural soils using phytoremediation (using Phaseolus vulgaris L.) and a locally adapted microbial consortium. J Environ Sci Health Part B 52(6):367–375

    Article  CAS  Google Scholar 

  • Mody B, Bindra M, Modi V (1989) Extracellular polysaccharides of cowpea rhizobia: compositional and functional studies. Arch Microbiol 153(1):38–42

    Article  CAS  Google Scholar 

  • Mondal NK, Das C, Roy S, Datta JK (2013) Effect of varying cadmium stress on chickpea (Cicer arietinum L.) seedlings: an ultrastructural study. Ann Environ Sci 7:59–70

    CAS  Google Scholar 

  • Nandula VK, Tyler HL (2016) Effect of new auxin herbicide formulations on control of herbicide resistant weeds and on microbial activities in the rhizosphere. Am J Plant Sci 7(17):429

    Article  Google Scholar 

  • Nguyen C, Yan W, Le Tacon F, Lapeyrie F (1992) Genetic variability of phosphate solubilizing activity by monocaryotic and dicaryotic mycelia of the ectomycorrhizal fungus Laccaria bicolor (Maire) PD Orton. Plant Soil 143(2):193–199

    Article  CAS  Google Scholar 

  • Nithyakalyani V, Kannan M, Anandan R (2016) Insecticide and salt tolerance of plant growth promoting root nodule bacteria. Int J Curr Microbiol App Sci 5(4):942–956

    Article  Google Scholar 

  • Osman MEH, Abo-Shady AM, El-Nagar MM (2016) Cyanobacterial Arthrospira (Spirulina platensis) as safener against harmful effects of fusilade herbicide on faba bean plant. Re Lincei 27(3):455–462

    Article  Google Scholar 

  • Pandey SP, Srivastava S, Goel R, Lakhwani D (2017) Simulated herbivory in chickpea causes rapid changes in defense pathways and hormonal transcription networks of JA/ethylene/GA/auxin within minutes of wounding. Sci Rep 7:44729

    Article  Google Scholar 

  • Park YG, Mun BG, Kang SM, Hussain A (2017) Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS ONE 12(3):e173203. 93–168

    Google Scholar 

  • Parsa M, Aliverdi A, Hammami H (2013) Effect of the recommended and optimized doses of haloxyfop-P-methyl or imazethapyr on soybean-Bradyrhizobium japonicum symbiosis. Ind Crops Prod 50:197–202

    Article  CAS  Google Scholar 

  • Penrose DM, Glick BR (2003) Method for isolating and characterizing ACC deaminase containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  Google Scholar 

  • Perez-Fernández M, Alexander V (2017) Enhanced plant performance in Cicer arietinum L. Due to the addition of a combination of plant growth-promoting bacteria. Agriculture 7(5):40

    Article  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorous in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370

    CAS  Google Scholar 

  • Premachandra D, Hudek L, Brau L (2016) Bacterial modes of action for enhancing of plant growth. J Biotechnol Biomater 6(3):1–8

    Google Scholar 

  • Premono ME, Moawad AM, Vlek PLG (1996) Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere

  • Raghavendra KS, Gundappagol RC, Santhosh GP (2017) Impact of herbicide application on beneficial soil microbial community, nodulation and yield parameters of chickpea (Cicer arietinum L.)

  • Rahman CH, Ahcene B, Miloud B, Rachid D (2017) Screening and characterization of plant growth promoting traits of phosphate solubilizing bacteria isolated from wheat rhizosphere of Algerian saline soil. Malays J Biol 13(2):124–131

    Google Scholar 

  • Rani R, Kumar V (2017) Endosulfan degradation by selected strains of plant growth promoting rhizobacteria. Bull Environ Contam Toxicol 99(1):138–145

    Article  CAS  Google Scholar 

  • Reeves MW, Pine L, Neilands JB, Balows A (1983) Absence of siderophore activity in Legionella species grown in iron-deficient media. J Bacteriol 154(1):324–329

    CAS  Google Scholar 

  • Rijavec T, Lapanje A (2016) Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol 7:1785

    Article  Google Scholar 

  • Rodríguez-Navarro DN, Rodríguez-Carvajal MA, Acosta-Jurado S (2014) Structure and biological roles of Sinorhizobium fredii HH103 exopolysaccharide. PLoS ONE 9(12):115391

    Article  Google Scholar 

  • Sadasivum S, Manickam A (1992) Biochemical methods. New Age International Publishers (P) Ltd., New Delhi

    Google Scholar 

  • Sahoo SK, Pradhan J, Kuruwanshi VB, Guhey A, Rout GR, Dash R (2017) Phytotoxic effect of pre-emergence herbicides on oil content and yield components of groundnut (Arachis hypogeae). Int J Curr Microbiol App Sci 6(9):1738–1748

    Article  Google Scholar 

  • Saleem S, Ahmed B, Khan MS, Al-Shaeri M, Musarrat J (2017) Inhibition of growth and biofilm formation of clinical bacterial isolates by NiO nanoparticles synthesized from Eucalyptus globulus plants. Microb Pathog. https://doi.org/10.1016/j.micpath.2017.09.019

    Google Scholar 

  • Sandanakirouchenane A, Haque E, Geetha T (2017) Recent studies on N2 fixing Burkholderia isolates as a biofertilizer for the sustainable agriculture. Int J Curr Microbiol App Sci 6(11):2780–2796

    Article  Google Scholar 

  • Sarkar A, Mukherjee PK, Bhattacharya PM (2005) Bio-efficacy of pendimethalin and fluchloralin in mustard. Ind J Weed Sci 37:275–276

    Google Scholar 

  • Shah S, Li J, Moffatt BA, Glick BR (1998) Isolation and characterization of ACC deaminase genes from two different plant growths promoting rhizobacteria. Can J Microbiol 44:833–843

    Article  CAS  Google Scholar 

  • Shahid M, Khan MS (2017) Assessment of glyphosate and quizalofop mediated toxicity to greengram [Vigna radiata (L.) Wilczek], stress abatement and growth promotion by herbicide tolerant Bradyrhizobium and Pseudomonas species. Int J Curr Microbiol App Sci 6(12):3001–3016

    Article  Google Scholar 

  • Sharma S, Verslues PE (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell Environ 33(11):1838–1851

    Article  CAS  Google Scholar 

  • Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600

    Google Scholar 

  • Sudharshana C, Prakash TR, Jayasree G, Reddy APK (2013) Effect of pendimethalin and imazethapyr on nodulation, nitrogen fixation and nitrogenase activity and yield in groundnut (Arachis Hypogaea L.). Int J Bioresour Stress Manag 4:309–313

    Google Scholar 

  • Tetard-Jones C, Edwards R (2016) Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci 72:203–209

    Article  CAS  Google Scholar 

  • Ugbe LA, Nadaeyo NU, Envyong JF (2016) Efficacy of selected herbicides on weed control, cowpea (Vigna unguiculata L. Walp) performance and economic returns in Akamkpa, Southeastern Nigeria. Int J Res Agri Forest 19:19–27

    Google Scholar 

  • Vogel C, Rehschuh S, Kemi Olagoke F (2017) Interactions between extracellular polymeric substances and clay minerals affect soil aggregation. In: 19th EGU General Assembly, EGU2017, proceedings from the conference held 23–28 April, 2017 in Vienna, Austria, p 18653

  • Yuan SL, Li R, Chen HF, Zhang CJ (2017) RNA-Seq analysis of nodule development at five different developmental stages of soybean (Glycine max) inoculated with Bradyrhizobium japonicum strain 113-2. Sci Rep 7:42248

    Article  CAS  Google Scholar 

  • Zablotowicz RM, Reddy KN (2007) Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Prot 26(3):370–376

    Article  CAS  Google Scholar 

  • Zeidan AA, Poulsen VK, Janzen T (2017) Polysaccharide production by lactic acid bacteria: from genes to industrial applications. FEMS Microbiol Rev 41(Supp_1):S168–S200. https://doi.org/10.1093/femsre/fux017

    Article  Google Scholar 

  • Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132(3):361–373

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Macrogen Seoul, Korea, for providing 16SrRNA gene Sequencing analysis and University Sophisticated Instrument facility (USIF) for providing SEM and CLSM facilities.

Funding

The author (Mohammad Shahid) would like to acknowledge the financial support received in the form of UGC Non-NET fellowship granted by University Grants Commission, New Delhi.

Author information

Authors and Affiliations

Authors

Contributions

MSK conceived and designed the experiments. MS performed the experiments and analyzed the data statistically. MS and MSK prepared the manuscript and approved the final draft.

Corresponding author

Correspondence to Mohammad Shahid.

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

Shahid, M., Khan, M.S. Glyphosate induced toxicity to chickpea plants and stress alleviation by herbicide tolerant phosphate solubilizing Burkholderia cepacia PSBB1 carrying multifarious plant growth promoting activities. 3 Biotech 8, 131 (2018). https://doi.org/10.1007/s13205-018-1145-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-018-1145-y

Keywords

Navigation