Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Influence of sub-lethal crude oil concentration on growth, water relations and photosynthetic capacity of maize (Zea mays L.) plants


Maize tolerance potential to oil pollution was assessed by growing Zea mays in soil contaminated with varying levels of crude oil (0, 2.5 and 5.0 % v/w basis). Crude oil contamination reduced soil microflora which may be beneficial to plant growth. It was observed that oil pollution caused a remarkable decrease in biomass, leaf water potential, turgor potential, photosynthetic pigments, quantum yield of photosystem II (PSII) (Fv/Fm), net CO2 assimilation rate, leaf nitrogen and total free amino acids. Gas exchange characteristics suggested that reduction in photosynthetic rate was mainly due to metabolic limitations. Fast chlorophyll a kinetic analysis suggested that crude oil damaged PSII donor and acceptor sides and downregulated electron transport as well as PSI end electron acceptors thereby resulting in lower PSII efficiency in converting harvested light energy into biochemical energy. However, maize plants tried to acclimate to moderate level of oil pollution by increasing root diameter and root length relative to its shoot biomass, to uptake more water and mineral nutrients.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9


  1. Adam G, Duncan H (2002) Influence of diesel fuel on seed germination. Environ Pollut 120:363–370

  2. Adenipekun CO, Oyetunji OJ, Kassim LS (2008) Effect of spent engine oil on the growth parameters and chlorophyll content of Corchorus olitorius Linn. Environmentalist 28:446–450

  3. Agbogidi OM (2011) Eco-toxicological effects of crude oil pollution on Rhizophora racemosa G. Mey J Sustainable Forest 30:713–720

  4. Agbogidi OM, Eruotor PG, Akparobi SO (2007a) Effects of crude oil levels on the growth of maize (Zea mays L.). Am J Food Technol 2:529–535

  5. Agbogidi OM, Eruotor PG, Akparobi SO, Nnaji GU (2007b) Evaluation of crude oil contaminated soil on the mineral nutrient elements of maize (Zea mays L.). J Agron 6:188–193

  6. Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds) Methods in plant ecology. Blackwell Scientific Publication, Oxford, pp 258–344

  7. Amakiri JO, Onofeghara FA (1983) Effect of crude oil pollution on the growth of Zea mays, Abelmoschus esculentus and Capsicum frutescens. Oil Petrochem Pollut 1:199–205

  8. Anoliefo GO, Vwioko DE (1995) Effects of spent lubricating oil on the growth of Capsicum annum L. and Lycopersicon esculentum Miller. Environ Pollut 88:361–364

  9. Anoliefo GO, Vwioko DE, Mpamah P (2003) Regeneration of Chromolaena odorata (L) K. & R. in crude oil polluted soil: a possible phytoremediating agent. Sci Digest 1:9–16

  10. Ashraf M, Rehman H-u (1999) Interactive effects of nitrate and long-term waterlogging on growth, water relations, and gaseous exchange properties of maize (Zea mays L.). Plant Sci 144:35–43

  11. Asuquo FE, Ibanga IJ, Idungafa N (2002) Effects of Qua Iboe (Nigerian) crude oil on germination and growth of okra (Abelmoschus essculentus L.) and fluted pumpkin (Telfairia occidentalis L.) in the tropics. J Environ Pollut Health 1:31–40

  12. Athar H-u-R, Bhatti AR, Bashir N, Zafar ZU, Abida FA (2011) Modulating infestation rate of white fly (Bemicia tabaci) on okra (Hibiscus esculentus L.) by nitrogen application. Acta Physiol Plant 33:843–850

  13. Athar HuR, Zafar ZU, Ashraf M (2015) Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators. J Agron Crop Sci 201:428–442

  14. Baek KH, Kim HS, Oh HM, Yoon BD, Kim J, Lee IS (2004) Effects of crude oil, oil components, and bioremediation on plant growth. J Environ Sci Health, Part A: Tox Hazard Subst Environ Eng 39:2465–2472

  15. Baker JM (1970) The effects of oils on plants. Environ Pollut 1:27–44

  16. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  17. Chen S, Kang Y, Zhang M, Wang X, Strasser RJ, Zhou B, Qiang S (2015) Differential sensitivity to the potential bioherbicide tenuazonic acid probed by the JIP-test based on fast chlorophyll fluorescence kinetics. Environ Exp Bot 112:1–15

  18. Chupakhina GN, Maslennikov PV (2004) Plant adaptation to oil stress. Russian J Ecol 35:290–295

  19. Cubera E, Moreno G, Solla A (2009) Quercus ilex root growth in response to heterogeneous conditions of soil bulk density and soil NH4-N content. Soil Till Res 103:16–22

  20. Davies WJ, Bacon MA (2003) Adaptation of roots to drought. In: de Kroon H, Visser EJW (eds) Root ecology. Springer-Verlag, Berlin, Heidelberg, pp 173–192

  21. Dorn PB, Salanitro JP (2000) Temporal ecological assessment of oil contaminated soils before and after bioremediation. Chemosphere 40:419–426

  22. Ebere JU, Wokoma EC, Wokocha CC (2011) Enhanced remediation of a hydrocarbon polluted soil. Res J Environ Earth Sci 3:70–74

  23. Ellis R, Adams RS (1961) Contamination of soils by petroleum hydrocarbons. Adv Agron 13:197–216

  24. Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31:713–727

  25. Gill LS, Nyawuame HGK, Ehikhametalor AO (1992) Effect of crude oil on the growth and anatomical features of Chromolaena odorata (L.) K. & R. Newsletter 6:1–6

  26. Guha A, Sengupta D, Reddy AR (2013) Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J Photochem Photobiol B Biol 119:71–83

  27. Hinsinger P, Bengough A, Vetterlein D, Young I (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

  28. Ibemesim RI (2010) Effect of salinity and Wytch farm crude oil on Paspalum conjugatum Bergius (sour grass). J Biol Sci 10:122–130

  29. Iwegbue CMA, Emuh FN, Isirimah NO, Egun AC (2007) Fractionation, characterization and speciation of heavy metals in composts and compost-amended soils. Afr J Biotechnol 6:67–78

  30. Kaczyńska G, Borowik A, Wyszkowska J (2015) Soil dehydrogenases as an indicator of contamination of the environment with petroleum products. Water Air Soil Pollut 226:1–11

  31. Khalid A, Athar H-u-R, Zafar ZU, Akram A, Hussain K, Manzoor H, Al-Qurainy F, Ashraf M (2015) Photosynthetic capacity of canola (Brassica napus L.) plants as affected by glycinebetaine under salt stress. J Appl Bot Food Qual 88:78–86

  32. Kirk JL, Klironomos JN, Lee H, Trevors JT (2005) The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ Pollut 133:455–465

  33. Lin Q, Mendelssohn IA, Suidan MT, Lee K, Venosa AD (2002) The dose-response relationship between No. 2 fuel oil and the growth of the salt marsh grass, Spartina alterniflora. Mar Pollut Bull 44:897–902

  34. Marti MC, Camejo D, Fernandez-Garcia N, Rellan-Alvarez R, Marques S, Sevilla F, Jimenez A (2009) Effect of oil refinery sludges on the growth and antioxidant system of alfalfa plants. J Hazard Mater 171:879–885

  35. Mathur S, Kalaji HM, Jajoo A (2016) Investigation of deleterious effects of chromium phytotoxicity and photosynthesis in wheat plant. Photosynthetica 54:185–192

  36. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

  37. Merkl N, Schultze-Kraft R, Infante C (2004) Phytoremediation in the tropics—the effect of crude oil on the growth of tropical plants. Bioremediation J 8:177–184

  38. Merkl N, Schultze-Kraft R, Infante C (2005a) Assessment of tropical grasses and legumes for phytoremediation of petroleum-contaminated soils. Water Air Soil Pollut 165:195–209

  39. Merkl N, Schultze-Kraft R, Infante C (2005b) Phytoremediation in the tropics—influence of heavy crude oil on root morphological characteristics of graminoids. Environ Pollut 138:86–91

  40. Naidoo G, Naidoo Y, Achar P (2010) Responses of the mangroves Avicennia marina and Bruguiera gymnorrhiza to oil contamination. Flora 205:357–362

  41. Njoku KL, Akinola MO, Oboh BO (2009) Phytoremediation of crude oil contaminated soil: the effect of growth of Glycine max on the physico-chemistry and crude oil contents of soil. Nat Sci 7:79–87

  42. Ogbo EM, Tabuanu A, Ubebe R (2007) Phytotoxicity assay of diesel fuel-spiked substrates remediated with Pleurotus tuberregium using Zea mays. Int J Appl Res Natur Prod 3:12–16

  43. Okonwu K, Amakiri JO, Etukudo MM, Osim SE, Mofunanya AAJ (2010) Growth and development response of maize (Zea mays L.) In crude oil pollution treatment. Global J Environ Sci 9:1–5

  44. Onyeneke EC, Aguebor-Ogie B (2007) Bonny light crude oil and its fractions alter radicle galactose dehydrogenase activity of beans (Phaseolus vulgaris L.) and maize (Zea mays). Trend Appl Sci Res 2:433–438

  45. Paulauskienė T, Jucikė I, Juščenko N, Baziukė D (2014) The use of natural sorbents for spilled crude oil and diesel cleanup from the water surface. Water Air Soil Pollut 225:1–12

  46. Peña-Castroa JM, Barrera-Figueroa BE, Fernández-Linaresb L, Ruiz-Medrano R, Xoconostle-Cázaresa B (2006) Isolation and identification of up-regulated genes in bermudagrass roots (Cynodon dactylon L.) grown under petroleum hydrocarbon stress. Plant Sci 170:724–731

  47. Pernar N, Baksic D, Antonic O, Grubesic M, Tikvic I, Trupcevic M (2006) Oil residuals in lowland forest soil after pollution with crude oil. Water Air Soil Pollut 177:267–284

  48. Pezeshki SR, Hester MW, Lin Q, Nyman JA (2000) The effects of oil spill and clean-up on dominant US Gulf coast marsh macrophytes: a review. Environ Pollut 108:129–139

  49. Razaq M, Haneef Q, Athar HR, Nasir M, Afzal M (2014) Interactive effect of nitrogen and insecticide on jassid, Amrasca devastans (Dist.) Population and photosynthetic capacity of okra Abelmoschus esculentus (L.) Moench. Pak J Zool 46:577–579

  50. Reilley KA, Banks MK, Schwab AP (1996) Dissipation of polycyclic aromatic hydrocarbons in the rhizosphere. J Environ Qual 25:212–219

  51. Rodríguez-Blanco A, Antoine V, Pelletier E, Delille D, Ghiglione J-F (2010) Effects of temperature and fertilization on total vs. active bacterial communities exposed to crude and diesel oil pollution in NW Mediterranean Sea. Environ Pollut 158:663–673

  52. Sharp RE, Silk WK, Hsiao TC (1988) Growth of the maize primary root at low water potentials.1. Spatial-distribution of expansive growth. Plant Physiol 87:50–57

  53. Snecdecor GW, Cochran WG (1989) Statistical methods. Iowa State University Press, Ames

  54. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

  55. Tomar RS, Jajoo A (2013) A quick investigation of the detrimental effects of environmental pollutant polycyclic aromatic hydrocarbon fluoranthene on the photosynthetic efficiency of wheat (Triticum aestivum). Ecotoxicology 22:1313–1318

  56. Tomar RS, Sharma A, Jajoo A (2015) Assessment of phytotoxicity of anthracene in soybean (Glycine max) with a quick method of chlorophyll fluorescence. Plant Biol 17:870–876

  57. Tsimilli-Michael M, Strasser R (2013) Biophysical phenomics: evaluation of the impact of mycorrhization with Piriformospora indica. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica. Soil Biology. Springer, Berlin Heidelberg, pp 173–190

  58. Wilson JR, Ludlow MM, Fisher MJ, Schulze E (1980) Adaptation to water stress of the leaf water relations of four tropical forage species. Funct Plant Biol 7:207–220

  59. Yasmeen A, Basra SMA, Farooq M, Rehman HU, Hussain N, Athar HUR (2013) Exogenous application of moringa leaf extract modulates the antioxidant enzyme system to improve wheat performance under saline conditions. Plant Growth Regul 69:225–233

  60. Yousaf S, Ripka K, Reichenauer TG, Andria V, Afzal M, Sessitsch A (2010) Hydrocarbon degradation and plant colonization by selected bacterial strains isolated from Italian ryegrass and birdsfoot trefoil. J Appl Microbiol 109:1389–1401

  61. Zafar ZU, Athar H-u-R (2013) Reducing disease incidence of cotton leaf curl virus (CLCuV) in cotton (Gossypium hirsutum L.) by potassium supplimentation. Pak J Bot 45:1029–1038

  62. Zafar ZU, Athar H-U-R, Ashraf M (2010) Responses of two cotton (Gossypium hirsutum L.) Cultivars differing in resistance to leaf curl virus disease to nitrogen nutrition. Pak J Bot 42:2085–2094

  63. Zhang Z, Gai L, Hou Z, Yang C, Ma C, Wang Z, Sun B, He X, Tang H, Xu P (2010) Characterization and biotechnological potential of petroleum-degrading bacteria isolated from oil-contaminated soils. Bioresour Technol 101:8452–8456

Download references

Author information

Correspondence to Habib-ur-Rehman Athar.

Ethics declarations

Authors’ contribution

Habib-ur-Rehman Athar and Zafar Ullah Zafar designed the experiment; Sarah Ambreen, Muhammad Javed, Mehwish Hina and Sumaira Rasul conducted the experiment; Muhammad Afzal did the soil analysis and microbial count; Habib-ur-Rehman Athar, Chukwuma C Ogbaga, Hamid Manzoor and Zafar Ullah Zafar did the physiological analysis; and Habib-ur-Rehman Athar, Fahad-Al-Qurainy and Muhammad Ashraf wrote and edited the manuscript. All authors agreed to submit this MS to Environmental Science and Pollution Research.

Additional information

Capsule abstract

Oil pollution reduced the maize growth by affecting water relations and thylakoidal and stromal reactions, but it increased root length and thus helped in regulation of water and N uptake during acclimation.


• Physiological and biochemical responses of Zea mays grown in soil contaminated with crude oil were assessed.

• Crude oil pollution reduced the growth of maize plants, which is mainly associated with reduction in plant water status, reduction in N accumulation, and reduced photosynthetic rate.

• Plants grown in soil contaminated with 2.5 % tried to acclimate by improving root traits.

• Gas exchange measurements evidenced that reduction in photosynthetic rate due to crude oil was due to non-stomatal factors.

• Fast chlorophyll a kinetic studies showed that reduction in quantum yield of PSII (F v/F m) was associated with PSII damage at both donor and acceptor side.

• Quenching analysis suggested that PSII damage might have been due to lower turnover of D1 protein.

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

(Supplementary information) Chlorophyll a transients in the leaves of three week old maize plants grown for further three weeks in soil contaminated with varying concentration of crude oil (v/w). a) raw curves; b) Fo normalized; c) Fm normalized ; d) double normalized curves. (XLSX 211 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Athar, H., Ambreen, S., Javed, M. et al. Influence of sub-lethal crude oil concentration on growth, water relations and photosynthetic capacity of maize (Zea mays L.) plants. Environ Sci Pollut Res 23, 18320–18331 (2016). https://doi.org/10.1007/s11356-016-6976-7

Download citation


  • JIP test, nitrogen
  • Oil pollution
  • PIABS, photosynthetic rate, water potential