Efficiency of biogas slurry and Burkholderia phytofirmans PsJN to improve growth, physiology, and antioxidant activity of Brassica napus L. in chromium-contaminated soil

Abstract

Contamination of soil is a major problem globally with colligated danger for ecosystem and human health. Chromium (Cr) is a toxic heavy metal and caused harmful effect on growth and development of plants. Phytostabilization reduced the mobility of heavy metals with addition of amendments which can significantly decrease metal solubility in soil. Phytostabilization can be achieved by application of biogas slurry (BGS) and endophytic bacteria as amendments in the contaminated soils. The present study revealed that the Burkholderia phytofirmans PsJN and BGS improved the growth, physiology, and antioxidant activity and reduced Cr uptake under a pot experiment spiked with Cr (20 mg kg−1 soil). The experiment was designed under completely randomized design, four treatments with three replications in normal and Cr-contaminated soil. The inoculation of endophytic bacteria improved the growth and physiology of Brassica. This study showed that the inoculation of endophytic bacteria stabilized the Cr levels in soil and minimized the uptake by the plant shoots and roots in BGS-amended soil. Similarly, activity of antioxidants such as catalase (CAT), reduced glutathione (GSH), glutathione peroxidase (GSH-Px), and glutathione s-transferase (GST) was decreased to normal with combined treatment of BGS and endophytic bacteria in Cr-stressed soil. Overall, the best results were analyzed by combined treatment of BGS and endophytic bacteria to improve growth, physiology, and antioxidant activity of Brassica and immobilize Cr in soil. Moreover, results emphasized the need to use BGS alone or in combination with endophytic bacteria to optimize crop performance, stabilize Cr concentration, and improve environmental efficiency.

This is a preview of subscription content, access via your institution.

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

References

  1. Abbas T, Rizwan M, Ali S, Adrees M, Rehman MZ, Qayyum F, Ok YS, Murtaza G (2017) Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ Sci Pollut Res Online. https://doi.org/10.1007/s11356-017-8987-4

  2. Adewuyi YG (2005a) Sonochemistry in environmental remediation. 1. Combinative and hybrid sonophotochemical oxidation processes for the treatment of pollutants in water. Environ Sci Technol 39(10):3409–3420. https://doi.org/10.1021/Es049138y

    CAS  Article  Google Scholar 

  3. Adewuyi YG (2005b) Sonochemistry in environmental remediation. 2. Heterogeneous sonophotocatalytic oxidation processes for the treatment of pollutants in water. Environ Sci Technol 39(22):8557–8570. https://doi.org/10.1021/es0509127

    CAS  Article  Google Scholar 

  4. Ahmad M, Zahir ZA, Nadeem SM, Nazli F, Jamil M, Jamshaid MU (2014) Physiological response of mung bean to Rhizobium and Pseudomonas based biofertilizers under salinity stress. Pak J Agric Sci 51:555–562

    Google Scholar 

  5. Akhtar MFZ, Jamil M, Ahamd M, Abbasi GH (2017) Evaluation of biofertilizer in combination with organic amendments and rock phosphate enriched compost for improving productivity of chickpea and maize. Soil Environ 36(1):59–69

    Google Scholar 

  6. Alamgir M, Kibria MG, Islam M (2011) Effects of farm yard manure on cadmium and lead accumulation in amaranth (Amaranthus oleracea L.) J Soil Sci Environ Manag 2(8):237–240

    Google Scholar 

  7. Ali S, Duan J, Charles TC, Glick BR (2013) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198

    Article  Google Scholar 

  8. Andaleeb F, Zia MA, Ashraf M, Khalid ZM (2008) Effect of chromium on growth attributes in sunflower (Helianthus annuus L.) J Environ Sci 20:1475–1480

    Article  Google Scholar 

  9. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55(1):373–399. https://doi.org/10.1146/ annurev.arplant.55.031903.141701

    CAS  Article  Google Scholar 

  10. Bacon M (2004) Water use efficiency in plant biology. Blackwell Publishing Ltd, Oxford ISBN 1-4051-1434-7. Print

    Google Scholar 

  11. Banks MK, Schwab AP, Henderson C (2006) Leaching and reduction of chromium in soil as affected by soil organic content and plants. Chemosphere 62(2):255–264. https://doi.org/10.1016/j.chemosphere.2005.05.020

    CAS  Article  Google Scholar 

  12. Ben-Amor N, Hamed KB, Debez A, Grignon C, Abdelly C (2005) Physiological and antioxidant response of the perennial halophytes Crithmum maritimum to salinity. Plant Sci 168(4):889–899. https://doi.org/10.1016/j.plantsci.2004.11.002

    CAS  Article  Google Scholar 

  13. Bharathi VA, Anand V, Shanthi SS, Hemalatha G (2016) Changes in antioxidant level in Macrotyloma uniflorum l. grown under lead toxicity. Int J Pharm Technol 8:18971–18977

    CAS  Google Scholar 

  14. Boshra AH, Khan AL, Waqas M, Al-Harrasia 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  Google Scholar 

  15. Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98(4):1222–1227. https://doi.org/10.1104/pp.98.4.1222

    CAS  Article  Google Scholar 

  16. Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, AitBarka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium, Burkholderia sp. strain PsJN. Appl Environ Microbiol 71(4):1685–1693. https://doi.org/10.1128/AEM.71.4.1685-1693.2005

    CAS  Article  Google Scholar 

  17. Dixon DP, Cummins L, Cole DJ, Edwards R (1998) Glutathione-mediated detoxifcation systems in plants. Curr Opin Plant Biol 1(3):258–266. https://doi.org/10.1016/S1369-5266(98)80114-3

    CAS  Article  Google Scholar 

  18. Dourado MN, Franco MR, Peters LP, Martins PF, Souza LA, Piotto FA, Azevedo RA (2015) Antioxidant enzymes activities of Burkholderia spp. strains—oxidative responses to Ni toxicity. Environ Sci Pollut Res 22(24):19922–19932. https://doi.org/10.1007/s11356-015-5204-1

    CAS  Article  Google Scholar 

  19. Dube BK, Tewari K, Chatterjee J, Chaterejee C (2003) Excess chromium alters uptake and translocation of certain nutrients in Citrullus. Chemosphere 53(9):1147–1153. https://doi.org/10.1016/S0045-6535(03)00570-8

    CAS  Article  Google Scholar 

  20. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root associated microbiomes of rice. Proc Nat Acad Sci. https://doi.org/10.1073/pnas.1414592112

  21. Fahim N, Naeem M, Ashraf MY, Tahir MN, Zulfiqar B, Salahuddin M, Shabbir RN, Aslam (2016) Selenium supplementation affects physiological and biochemical processes to improve fodder yield and quality of maize (Zea mays L.) under water deficit conditions. Front Plant Sci

  22. Farid M, Ali S, Rizwan M, Ali Q, Abbas F, Bukhari SAH, Saeed R, Wu L (2017) Citric acid assisted phytoextraction of chromium by sunflower; morpho-physiological and biochemical alterations in plants. Ecotox Environ Safe 145:90–102

    CAS  Article  Google Scholar 

  23. Faryal RF, Tahir F, Hameed A (2007) Effect of wastewater irrigation on soil along with its micro and macro flora. Pak J Bot 39:193–204

    Google Scholar 

  24. Fein JB, Kemner K, Fowle DA, Cahill J, Boyanov M, Bunker B (2001) Non metabolic reduction of Cr(VI) by bacterial surfaces under nutrient-absent conditions. Geomicrobiol J (in press)

  25. Frey-Klett P, Churin JL, Pierrat JC, Garbaye J (1999) Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biol Biochem 31(11):1555–1562. https://doi.org/10.1016/S0038-0717(99)00079-6

    CAS  Article  Google Scholar 

  26. Frommel MI, Nowak J, Lazarovits G (1991) Growth enhancement and development modifications of invitro grown potato (Solanum tuberosum sp.) as affected by a non-fluorescent Pseudomonas sp. Plant Physiol 96(3):928–936. https://doi.org/10.1104/pp.96.3.928

    CAS  Article  Google Scholar 

  27. Gamalero E, Glick BR (2011) Mechanism used by plant growth promoting bacteria. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 17–46

    Google Scholar 

  28. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 246:7130–7139

    Google Scholar 

  29. Hasanuzzaman M, Hossain MA, Jaime A, da Silva T, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop Stress and its Management: Perspectives and Strategies. Springer, Berlin, pp 261–316. https://doi.org/10.1007/978-94-007-2220-0_8

    Google Scholar 

  30. Hoffmann MR, Hua I, Hochemer R (1996) Application of ultrasonic irradiation for the degradation of chemical contaminants in water. Ultrason Sonochem 3(3):163–172. https://doi.org/10.1016/S1350-4177(96)00022-3

    Article  Google Scholar 

  31. Holman HYN, Perry DL, Martin MC, Lamble G, McKinney WR, Hunter Cevera JC (1999) Real-time characterization of biogeochemical reduction of Cr(VI) on basalt surfaces by SR-FTIR imaging. Geomicrobiol J 16:307–323

    CAS  Article  Google Scholar 

  32. Huang L, Yang J, Gao W, Yang W, Cui X, Zhuang H (2016) Effects of pig slurry as basal and panicle fertilizer on trace element content and grain quality in direct-seeding rice. Sustainability 8(8):714. https://doi.org/10.3390/su8080714

    Article  Google Scholar 

  33. Islam F, Yasmeen T, Ali Q, Mubin M, Ali S, Arif MS, Hussain S, Riaz M, Abbas F (2015a) Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environ Sci Pollut Res 23:220–233

    Article  Google Scholar 

  34. Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou W (2015b) Plant growth promoting bacteria confer salt tolerance in Vigna radiate by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul 80:23–36

    Article  Google Scholar 

  35. Jones JB, Case VW (1990) Sampling, handling and analyzing plant tissue samples. In: Westerman RL (ed) Soil testing and plant analysis, 3rd edn. Soil Science Society of America, Book Series No. 3, Madison, pp 389–427

    Google Scholar 

  36. Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12(12):6894–6918. https://doi.org/10.3390/ijms12106894

    CAS  Article  Google Scholar 

  37. Khan MA, Shaukat SS, Khan MA (2008) Economic benefits from irrigation of maize with treated effluent of waste stabilization pond. Pak J Bot 40:1091–1098

    Google Scholar 

  38. Krishna KR, Philip L (2005) Bioremediation of Cr (VI) in contaminated soils. J Hazard Mater 121(1-3):109–111. https://doi.org/10.1016/j.jhazmat.2005.01.018

    CAS  Article  Google Scholar 

  39. Kurepin LV, Pharis RP (2014) Light signaling and the phyto hormonal regulation of shoot growth. Plant Sci 229:280–228. https://doi.org/10.1016/j.plantsci.2014.10.006

    CAS  Article  Google Scholar 

  40. Kurepin LV, Zaman M, Pharis RP (2014) Phytohormonal basis for the plant growth promoting action of naturally occurring bio-stimulators. J Sci Food Agric 95:1715–1722

    Article  Google Scholar 

  41. Kurepin LV, Park JM, Lazarovits G, Norman PA, Huner (2015) Involvement of plant stress hormones in Burkholderia phytofirmans induced shoot and root growth promotion. Plant Growth Regul 77(2):179–187. https://doi.org/10.1007/s10725-015-0049-7

    CAS  Article  Google Scholar 

  42. Lin WH, Wang JJ, Li HQ, Zhang GM, Tian P (2016) Effects of endophytic fungi on perennial rye grass physiological characteristics under different growth conditions. Pratacul Sci 33:1574–1582

    Google Scholar 

  43. Losi ME, Amrhein C, Frankenberger WT (1994) Factors affecting chemical and biological reduction of Cr (VI) in soil. Environ Toxicol Chem 13(11):1727–1735. https://doi.org/10.1002/etc.5620131103

    CAS  Article  Google Scholar 

  44. Mandal KG, Sinha AC (2004) Nutrient management effects on light interception, photosynthesis, growth, dry matter production and yield of Indian mustard (Brassica juncea). J Agron Crop Sci 190(2):119–129. https://doi.org/10.1046/j.1439-037X.2003.00083.x

    CAS  Article  Google Scholar 

  45. Meunchang S, Panichsakpatana S, Weaver RW (2005) Co-composting of filter cake and bagasse; byproducts from a sugar mill. Bioresour Technol 96(4):437–442. https://doi.org/10.1016/j.biortech.2004.05.024

    CAS  Article  Google Scholar 

  46. Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Teodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133(2):443–447. https://doi.org/10.1104/pp.103.028399

    CAS  Article  Google Scholar 

  47. Mitter B, Petric A, Shin MW, Chain PSG, Hauberg-Lotte L, Reinhold-Hurek B, Nowak J, Sessitsch A (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120

    Article  Google Scholar 

  48. Montes-Holguin MO, Peralta-Videa JR, Meitzner G, Martinez-Martinez A, de la Rosa G, Castillo-Michel HA, Gardea-Torresdey JL (2006) Biochemical and spectroscopic studies of the response of Convolvulus arvensis L. to chromium (III) and chromium (VI) stress. Environ Toxicol Chem 25(1):220–226. https://doi.org/10.1897/05-089R.1

    CAS  Article  Google Scholar 

  49. Moron MS, De Pierre JW, Vik BM (1979) Levels of glutathione, glutathione reductase and glutathione-S-transferase activities in rat and lung liver. Biochem Biophys Acta 582:3170–3185

    Article  Google Scholar 

  50. Mulligan CN, Young R, Gibbs B (2001) Remediation technologies for metal contaminated soils and ground water: an evaluation. Eng Geol 60(1-4):193–207. https://doi.org/10.1016/S0013-7952(00)00101-0

    Article  Google Scholar 

  51. Naveed M, Mittera B, Reichenauerb TG, Wieczorekc K, Sessitscha A (2014a) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39. https://doi.org/10.1016/j.envexpbot.2013.09.014

    CAS  Article  Google Scholar 

  52. Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014b) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73(2):121–131. https://doi.org/10.1007/s10725-013-9874-8

    CAS  Article  Google Scholar 

  53. Nouairi I, Ammar WB, Youssef NB, Ben Miled DD, Ghobal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica nepus) under cadmium stress. Acta Physiol Plant 31(2):237–247. https://doi.org/10.1007/s11738-008-0224-9

    CAS  Article  Google Scholar 

  54. Oseni OM, Adelusi AA, Dada EO et al (2016) Effects of heavy metal (Pb) concentration on some growth parameters of plants grown in lead polluted soil under organic fertilizer amendment. Sci Cold Arid Regions 8:0036–0045. https://doi.org/10.3724/SP.J.1226.2016.00036

    Google Scholar 

  55. Panagos P, van Liedekerke M, Yigini Y, Montanarella L (2013) Contaminated sites in Europe: review of the current situation based on data collected through a European network. J Environ Pub Health 11

  56. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Nat Acad Sci 110(16):6548–6553. https://doi.org/10.1073/pnas.1302837110

    CAS  Article  Google Scholar 

  57. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aus J Bot 61(3):167–234. https://doi.org/10.1071/BT12225

    Article  Google Scholar 

  58. 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(11):789–799. https://doi.org/10.1038/nrmicro3109

    CAS  Article  Google Scholar 

  59. Ponder SM, Darab JG, Mallouk TE (2000) Remediation of Cr(VI) and Pb(II) aqueous solutions using supported, nanoscale zero-valent iron. Environ Sci Technol 34(12):2564–2569. https://doi.org/10.1021/es9911420

    CAS  Article  Google Scholar 

  60. Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224. https://doi.org/10.1016/j.apsoil.2011.09.011

    Article  Google Scholar 

  61. Rehman MZ, Rizwan M, Ali S, Sabir M, Sohail MI (2017) Contrasting effects of organic and inorganic amendments on reducing lead toxicity in wheat. Bull Environ Contam Toxicol Online 99(5):642–647. https://doi.org/10.1007/s00128-017-2177-4

    Article  Google Scholar 

  62. Sekmen AH, Türkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131(3):399–411. https://doi.org/10.1111/j.1399-3054.2007.00970.x

    CAS  Article  Google Scholar 

  63. Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, Najeeb U, Bharwana SA, Abbasi GH (2014) Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotoxicol Environ Saf 109:38–47. https://doi.org/10.1016/j.ecoenv.2014.07.033

    Article  Google Scholar 

  64. Shankar AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 1:739–753

    Article  Google Scholar 

  65. Singh A, Agrawal M (2013) Reduction in metal toxicity by applying different soil amendments in agricultural field and its consequent effects on characteristics of radish plants (Raphanus sativus L.) J Agric Sci Technol 15:1553–1564

    CAS  Google Scholar 

  66. Singh G, Brar MS, Malhi S (2007) Decontamination of chromium by farm yard manure application in spinach grown in two texturally different Cr–contaminated soils. J Plant Nutr 30(2):289–308. https://doi.org/10.1080/01904160601118125

    CAS  Article  Google Scholar 

  67. Singh A, Agrawal M, Marshall F (2010) The role of organic vs. inorganic fertilizers in reducing phytoavailability of heavy metals in a wastewater-irrigated area. Ecol Eng 36(12):1733–1740. https://doi.org/10.1016/j.ecoleng.2010.07.021

    Article  Google Scholar 

  68. Sinha S, Saxena R, Singh S (2005) Chromium induced lipid peroxidation in the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58(5):595–604. https://doi.org/10.1016/j.chemosphere.2004.08.071

    CAS  Article  Google Scholar 

  69. Srivalli B, Chinnusamy V, Khanna-Chopra R (2003) Antioxidant defense in response to abiotic stresses in plants. J Plant Biol 30:121–139

    Google Scholar 

  70. Touceda-Gonzalez M, Brader G, Antonielli L, Ravindran VB, Waldner G, Hanl WF, Corretto E, Campisano A, Pancher M, Sessitsch A (2015) Combined amendment of immobilizers and the plant growth-promoting strain Burkholderia phytofirmans PsJN favours plant growth and reduces heavy metal uptake. Soil Biol Biochem 91:140–150. https://doi.org/10.1016/j.soilbio.2015.08.038

    CAS  Article  Google Scholar 

  71. U.S. EPA Method 7196A (1992) Chromium, Hexavalent (Colorimetric), SW-846 Third Edition, Update V. U.S. Government Printing Office, Washington DC http://www3.epa.gov/epawaste/hazard/testmethods/sw846/pdfs/7196a.pdf

  72. USEPA 3050B (1996) Acid digestion of sediments, sludge’s and soils. Environmental Protection Agency, Washington, DC

    Google Scholar 

  73. Vital SA, Fowler RW, Virgen A, Gossett DR, Banks SW, Rodriguez J (2008) Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue. Environ Exp Bot 62(1):60–68. https://doi.org/10.1016/j.envexpbot.2007.07.006

    CAS  Article  Google Scholar 

  74. Waqas M, Khan AL, Hamayun M, Shahzad R, Kim YH, Choi KS, Lee IJ (2014) Endophytic infection alleviates biotic stress in sunflower through regulation of defense hormones, antioxidants and functional amino acids. Eur J Plant Pathol 141(4):803–824. https://doi.org/10.1007/s10658-014-0581-8

    Article  Google Scholar 

  75. Wei Z, Spinney R, Ke R, Yang Z, Xiao Z (2016) Effect of pH on the sonochemical degradation of organic pollutants. Environ Chem Lett 14(2):163–182. https://doi.org/10.1007/s10311-016-0557-3

    CAS  Article  Google Scholar 

  76. Wendel A (1980) Glutathione peroxidases. In: Jakoby WB (ed) Enzymatic basis of detoxification. Academic Press, New York, pp 333–353. https://doi.org/10.1016/B978-0-12-380001-5.50022-0

    Google Scholar 

  77. Yang Z, Liu L, Chai L, Liao Y, Yao W, Xiao R (2015) Arsenic immobilization in the contaminated soil using poorly crystalline Fe-oxyhydroxy sulfate. Environ Sci Pollut Res 22(16):12624–12632. https://doi.org/10.1007/s11356-015-4455-1

    CAS  Article  Google Scholar 

  78. Yang Z, Zhang Z, Chai L, Wang Y, Liu Y, Xiao R (2016) Bioleaching remediation of heavy metal contaminated soils using Burkholderia sp.Z-90. J Hazard Mat 301:145–152. https://doi.org/10.1016/j.jhazmat.2015.08.047

    CAS  Article  Google Scholar 

  79. Zahir ZA, Zafar-ul-Hye M, Sajjad S, Naveed M (2011) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC deaminase for co-inoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biol Fertil Soil 47(4):457–465. https://doi.org/10.1007/s00374-011-0551-7

    CAS  Article  Google Scholar 

  80. Zhou Q (2009) Effect of BGS application on yield, nutrition quality of purple cabbage and soil quality. Acta Agric Jiangxi 2:07–27

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan; Austrian Institute of technology (AIT) for providing Burkholderia phytofirmans PsJN; and the Higher Education Commission (HEC) of Pakistan for providing financial support and research facilities.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shafaqat Ali.

Additional information

Responsible editor: Elena Maestri

Electronic supplementary material

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nafees, M., Ali, S., Naveed, M. et al. Efficiency of biogas slurry and Burkholderia phytofirmans PsJN to improve growth, physiology, and antioxidant activity of Brassica napus L. in chromium-contaminated soil. Environ Sci Pollut Res 25, 6387–6397 (2018). https://doi.org/10.1007/s11356-017-0924-z

Download citation

Keywords

  • Biogas slurry
  • Burkholderia phytofirmans PsJN
  • Antioxidants activity
  • Brassica napus L