Skip to main content

Advertisement

SpringerLink
Log in

Responses of Zea mays L. cultivars ‘Buland’ and ‘Prakash’ to an antiozonant ethylene diurea grown under ambient and elevated levels of ozone

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Increase in surface level of ozone (O3) in last 30 years is one of the major problems for global agriculture. Field experiment was conducted using open top chambers on two Indian maize cultivars (Buland and Prakash) grown under ambient (AO) and elevated (EO) O3 concentrations to evaluate the effect of an antiozonant ethylene diurea (EDU) given as soil drench. EDU application reduced the ROS production with concomitant decrease in lipid peroxidation. Inductions in activities of enzymatic antioxidants along with increased content of non-enzymatic antioxidants were observed in EDU-treated plants, though the response varied between the cultivars. Photosynthetic proteins (PEP carboxylase and RuBisCO large and small subunits) detected through SDS–PAGE analysis increased with EDU treatment. EDU also led to an increase in jasmonic acid and a decline in salicylic acid contents. The protective effect of EDU was further accompanied by increased pigments (chlorophyll and carotenoids), foliar carbohydrates (starch and total soluble sugars), enhanced biomass, and economic yield. Effectiveness of EDU was more evident at higher O3 concentration and cultivar Prakash exhibited a more positive response with EDU as compared to Buland.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

AOT40:

Accumulated ozone exposure above threshold of 40 ppb

APX:

Ascorbate peroxidase

CAT:

Catalase

DAG:

Days after germination

GR:

Glutathione reductase

GSH:

Reduced glutathione

H2O2 :

Hydrogen peroxide

LPO:

Lipid peroxidation

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NFC:

Non-filtered chamber

O2 ·− :

Superoxide radical

OTC:

Open top chamber

PEPC:

Phosphoenol pyruvate carboxylase

POX:

Peroxidase

ROS:

Reactive oxygen species

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SDS–PAGE:

Sodium dodecyl sulphate polyacrylamide gel electrophoresis

SOD:

Superoxide dismutase

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Agathokleous E, Saitanis CJ, Papatheohari Y (2014) Evaluation of Di-1-p-menthene as antiozonant on Bel-W3 tobacco plants, as compared with Ethylenediurea. Water Air Soil Pollut 225:1–4

    Article  CAS  Google Scholar 

  • Agathokleous E, Paoletti E, Saitanis CJ, Manning WJ, Shi C, Koike T (2016a) High doses of ethylene diurea (EDU) are not toxic to willow and act as nitrogen fertilizer. Sci Total Environ 566:841–850

    Article  PubMed  Google Scholar 

  • Agathokleous E, Mouzaki-Paxinou AC, Saitanis CJ, Paoletti E, Manning WJ (2016b) The first toxicological study of the antiozonant and research tool ethylene diurea (EDU) using a Lemna minor L. bioassay: hints to its mode of action. Environ Pollut 213:996–1006

    Article  CAS  PubMed  Google Scholar 

  • Agrawal M, Singh B, Rajput M, Marshall F, Bell JNB (2003) Effect of air pollution on peri-urban agriculture: a case study. Environ Pollut 126:323–329

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA, Yendrek CR, Sitch S, Collins WJ, Emberson LD (2012) The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 63:637–661

    Article  CAS  PubMed  Google Scholar 

  • Alexiva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  Google Scholar 

  • Al-Qurainy FH (2008) Effect of air pollution and ethylenediurea on broad bean plants grown at two localities in KSA. Int J Bot 4:117–122

    Article  CAS  Google Scholar 

  • Astorino G, Margani I, Tripodo P (1995) The response of Phaseolus vulgaris L. cv. Lit. to different dosages of the anti-ozonant ethylenediurea (EDU) in relation to chronic treatment with ozone. Plant Sci 111:237–248

    Article  CAS  Google Scholar 

  • Avnery S, Mauzerall DL, Liu J, Horowitz LW (2011) Global crop yield reductions due to surface ozone exposure: 1. Year 2000 crop production losses and economic damage. Atmos Environ 45:2284–2296

    Article  CAS  Google Scholar 

  • Booker F, Muntifering R, McGrath M, Burkey K, Decoteau D, Fiscus E, Manning W, Krupa S, Chappelka A, Grantz D (2009) The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. J Integr Plant Biol 5:337–351

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bray HG, Thorpe WY (1954) Analysis of phenolic compounds of interest in metabolism. In: Click D (ed) Methods of biochemical analysis, 1st edn. Interscience Publications Inc., New York, pp 27–52

    Google Scholar 

  • Britton C, Mehley AC (1955) Assay of catalase and peroxidase. In: Colowick SP, Kalpan NO (eds) Method in enzymology, vol 2. Academic, New York, pp 764–775

    Google Scholar 

  • Burkey KO, Eason G, Fiscus EL (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiol Plant 117:51–57

    Article  CAS  Google Scholar 

  • Carnahan JE, Jenner EL, Wat EKW (1978) Prevention of ozone injury in plants by a new protective chemical. Phytopathol 68:1225–1229

    Article  CAS  Google Scholar 

  • Chaudhary N, Agrawal SB (2013) Intraspecific responses of six Indian clover cultivars under ambient and elevated levels of ozone. Environ Sci Pollut Res 20:5318–5329

    Article  CAS  Google Scholar 

  • Choudhary KK, Agrawal SB (2014) Cultivar specificity of tropical mung bean (Vigna radiata L.) to elevated ultraviolet-B: changes in antioxidative defense system, nitrogen metabolism and accumulation of jasmonic and salicylic acids. Environ Exp Bot 99:122–132

    Article  CAS  Google Scholar 

  • Cooper OR, Parrish DD, Stohl A, Trainer M, Nedelec P, Thouret V, Cammas JP, Oltmans SJ, Johnson BJ, Tarasick D, Leblanc T, McDermid IS, Jaffe D, Gao R, Stith J, Ryerson T, Aikin K, Campos T, Weinheimer A, Avery MA (2010) Increasing spring time ozone mixing ratios in the free troposphere over western North America. Nature l463:344–348

    Article  Google Scholar 

  • Dentener F, Stevenson D, Cofala J, Mechler R, Amann M, Bergamaschi P, Raes F, Derwent R (2005) The impact of air pollutant and methane emission controls on tropospheric ozone and radiative forcing: CTM calculations for the period 1990–2030. Atmos Chem Phys 5:1731–1755

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Roberts PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Duxbury AC, Yentsch CS (1956) Plankton pigment monographs. J Mar Res 15:90–101

    Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Emberson LD, Büker P, Ashmore MR, Mills G, Jackson LS, Agrawal M, Atikuzzaman MD, Cinderby S, Engardt M, Jamir C, Kobayashi K (2009) A comparison of North American and Asian exposure-response data for ozone effects on crop yields. Atmos Environ 43:1945–1953

    Article  CAS  Google Scholar 

  • Fahey RC, Brown WC, Adams WB, Worsham MB (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Z, Wang S, Szantoi Z, Chen S, Wang X (2010) Protection of plants from ambient ozone by applications of ethylenediurea (EDU): a meta-analytic review. Environ Pollut 158:3236–3242

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (1974) Superoxide dismutase. Adv Enzymol 41:35–97

    CAS  PubMed  Google Scholar 

  • Harfouche AL, Rugini E, Mencarelli F, Botondi R, Mulco R (2008) Salicylic acid induces H2O2 production and endochitinase gene expression but not ethylene biosynthesis in Castanea sativa in vitro model system. J Plant Physiol 165:734–744

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Herbart D, Philipps PJ, Strange RE (1971) Estimation of reducing sugars. In: Noorier JR, Robbins DW (eds) Methods in microbiology, 10. Academic Press, Cap III, London, pp 209–344

    Google Scholar 

  • Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44

    Article  CAS  Google Scholar 

  • Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J Forest Pathol 7:338–350

    Article  CAS  Google Scholar 

  • Larson RA (1988) The antioxidants of higher plants. Phytochemistry 27:969–978

    Article  CAS  Google Scholar 

  • Lee EH, Bennett JH (1982) Superoxide dismutase: a possible protective enzyme against O3 injury in snap beans (Phaseolus vulgaris L.). Plant Physiol 69:1444–1449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee EH, Chen CM (1982) Studies on the mechanisms of ozone tolerance: cytokinin-like activity of N-[2-(2-oxo-1-imidazolidinyl) ethyl]-N′-phenylurea, a compound protecting against ozone injury. Physiol Plantarum 56:486–491

    Article  CAS  Google Scholar 

  • Lee EH, Bennett JH, Heggestad HE (1981) Retardation of senescence in red clover leaf discs by a new antiozonant EDU, N-[2-(2-oxo-1-imidazolidinyl) ethyl]-N-phenylurea. Plant Physiol 67:347–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee EH, Upadhyay A, Agrawal M, Rowland RA (1997) Mechanism of ethylenediurea (EDU) induced ozone protection: re-examination of free radical scavenger systems in snap bean exposed to O3. Environ Exp Bot 38:199–209

    Article  CAS  Google Scholar 

  • Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of a chlorophyll mutant of barley. Can J Bot 41:1053–1062

    Article  CAS  Google Scholar 

  • Manning WJ, Paoletti E, Sandermann H Jr, Ernst D (2011) Ethylenediurea (EDU): a research tool for assessment and verification of the effects of ground level ozone on plants under natural condition. Environ Pollut 159:3283–3293

    Article  CAS  PubMed  Google Scholar 

  • Mauzerall DL, Wang X (2001) Protecting agricultural crops from the effects of tropospheric ozone exposure: reconciling science and standard setting in United States, Europe and Asia. Ann Rev Energy Environ 26:237–287

    Article  Google Scholar 

  • Mishra AK, Agrawal SB (2015) Biochemical and physiological characteristics of tropical mung bean (Vigna radiata L.) cultivars against chronic ozone stress: an insight to cultivar-specific response. Protoplasma 252:797–811

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Orvar BL, McPherson J, Ellis BE (1997) Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J 11:203–212

    Article  CAS  PubMed  Google Scholar 

  • Pandey AK, Majumder B, Keski-Saari S, Kontunen-Soppela S, Pandey V, Oksanen E (2014) Differences in responses of two mustard cultivars to ethylenediurea (EDU) at high ambient ozone concentrations in India. Agr Ecosyst Environ 196:158–166

    Article  CAS  Google Scholar 

  • Pandey AK, Majumder B, Keski-Saari S, Kontunen-Soppela S, Mishra A, Sahu N, Pandey V, Oksanen E (2015) Searching for common responsive parameters for ozone tolerance in 18 rice cultivars in India: results from ethylenediurea studies. Sci Total Environ 532:230–238

    Article  CAS  PubMed  Google Scholar 

  • Paoletti E, Contran N, Manning WJ, Ferrara AM (2009) Use of antiozonant ethylenediurea (EDU) in Italy: verification of the effects of ambient ozone on crop plants and trees and investigation of EDU’s mode of action. Environ Pollut 157:1453–1460

    Article  CAS  PubMed  Google Scholar 

  • Paoletti E, Castagna A, Ederli L, Pasqualini S, Ranieri A, Manning WJ (2014) Gene expression in snapbeans exposed to ozone and protected by ethylenediurea. Environ Pollut 193:1–5

    Article  CAS  PubMed  Google Scholar 

  • Rai R, Agrawal M, Choudhary KK, Agrawal SB, Emberson L, Büker P (2015) Application of ethylene diurea (EDU) in assessing the response of a tropical soybean cultivar to ambient O3: nitrogen metabolism, antioxidants, reproductive development and yield. Ecotoxicol Environ Safe 112:29–38

    Article  CAS  Google Scholar 

  • Saitanis CJ, Bari SM, Burkey KO, Stamatelopoulos D, Agathokleous E (2014) Screening of Bangladeshi winter wheat (Triticum aestivum L.) cultivars for sensitivity to ozone. Environ Sci Pollut Res 21:13560–13571

    Article  CAS  Google Scholar 

  • Sarkar A, Singh AA, Agrawal SB, Ahmad A, Rai SP (2015) Cultivar specific variations in antioxidative defense system, genome and proteome of two tropical rice cultivars against ambient and elevated ozone. Ecotox Environ Safe 115:101–111

    Article  CAS  Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant physiol 59:1011–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh S, Agrawal SB (2009) Use of ethylenediurea (EDU) in assessing the impact of ozone on growth and productivity of five cultivars of Indian wheat (Triticum aestivum L.). Environ Monit Assess 159:125–141

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Agrawal SB (2010) Impact of tropospheric ozone on wheat (Triticum aestivum L.) in the eastern Gangetic plains of India as assessed by ethylenediurea (EDU) application during different developmental stages. Agric Ecosys Environ 138:214–221

    Article  CAS  Google Scholar 

  • Singh S, Agrawal SB (2011) Cultivar specific response of soybean (Glycine max. L) to ambient and elevated concentrations of ozone under open top chamber. Water Air Soil Pollut 217:283–302

    Article  CAS  Google Scholar 

  • Singh S, Agrawal SB, Agrawal M (2009) Differential protection of ethylenediurea against ambient ozone for five cultivars of tropical wheat. Environ Pollut 157:2359–2367

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Agrawal SB, Singh P, Agrawal M (2010a) Screening three cultivars of Vigna mungo L. against ozone by application of ethylenediurea (EDU). Ecotoxicol Environ Saf 73:1765–1775

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Agrawal M, Agrawal SB, Emberson L, Buker P (2010b) Use of ethylenediurea for assessing the impact of ozone on mungbean plants at a rural site in a dry tropical region of India. Int J Environ Waste Manag 5:125–139

    Article  CAS  Google Scholar 

  • Singh AA, Agrawal SB, Shahi JP, Agrawal M (2014a) Assessment of growth and yield losses in two Zea mays L. cultivars (quality protein maize and non quality protein maize) under projected levels of ozone. Environ Sci Pollut Res 21:2628–2641

    Article  CAS  Google Scholar 

  • Singh AA, Agrawal SB, Shahi JP, Agrawal M (2014b) Investigating the response of tropical maize (Zea mays L.) cultivars against elevated levels of O3 at two developmental stages. Ecotoxicology 23:1447–1463

    Article  CAS  PubMed  Google Scholar 

  • Singh AA, Singh S, Agrawal M, Agrawal SB (2015) Assessment of ethylene diurea-induced protection in plants against ozone phytotoxicity. Whitacre DM (ed) Rev Environ Cont Toxicol, vol 233, pp 129–184

  • Tiwari S, Agrawal M (2010) Effectiveness of different EDU concentrations in ameliorating ozone stress in carrot plants. Ecotoxicol Environ Saf 73:1018–1027

    Article  CAS  PubMed  Google Scholar 

  • Tonneijck AEG, VanDijk CJ (1997) Assessing the effects of ambient ozone on injury and growth of Trifolium subterraneum at four rural sites in the Netherlands with ethylene diurea (EDU). Agric Ecosyst Environ 65:79–88

    Article  CAS  Google Scholar 

  • Van Dingenen R, Dentener FJ, Raes F, Korl MC, Emberson L, Cofala J (2009) The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmos Environ 43:604–618

    Article  Google Scholar 

  • Wang X, Zheng Q, Yao F, Chen Z, Feng Z, Manning WJ (2007) Assessing the impact of ambient ozone on growth and yield of rice (Oryza sativa L.) and wheat (Triticum aestivum L.) cultivar grown in the Yangtze delta, China, using three rates of application of ethylenediurea (EDU). Environ Pollut 148:390–395

    Article  CAS  PubMed  Google Scholar 

  • Whitaker BD, Lee EH, Rowland RA (1990) EDU and O3 production: foliar glycerolipids and steryl lipids in snap bean exposed to O3. Physiol Plant 80:286–293

    Article  CAS  Google Scholar 

  • Wilkinson S, Mills G, Illidge R, Davies WJ (2011) How is ozone pollution reducing our food supply? J Exp Bot 63:527–536

    Article  PubMed  Google Scholar 

  • Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193:372–376

    Article  CAS  Google Scholar 

  • Yuan X, Calatayud V, Jiang L, Manning WJ, Hayes F, Tian Y, Feng Z (2015) Assessing the effects of ambient ozone in China on snap bean genotypes by using ethylenediurea (EDU). Environ Pollut 205:199–208

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Authors are grateful to the Head and Coordinator CAS, Department of Botany, Institute of Science, Banaras Hindu University for providing all the necessary laboratory and field facilities and to Council of Scientific and Industrial Research (CSIR) and UPE-University Grants Commission, ISLS (Department of Biotechnology), Science and Engineering Research Board (SERB-DST), and FIST (Department of Science and Technology), Government of India for the financial support.

Author information

Authors and Affiliations

  1. Laboratory of Air Pollution and Global Climate Change, Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Aditya Abha Singh, Meenakshi Chaurasia, Vaishali Gupta, Madhoolika Agrawal & S. B. Agrawal

Authors
  1. Aditya Abha Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meenakshi Chaurasia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vaishali Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Madhoolika Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. B. Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. B. Agrawal.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Z. Miszalski.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, A.A., Chaurasia, M., Gupta, V. et al. Responses of Zea mays L. cultivars ‘Buland’ and ‘Prakash’ to an antiozonant ethylene diurea grown under ambient and elevated levels of ozone. Acta Physiol Plant 40, 92 (2018). https://doi.org/10.1007/s11738-018-2666-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2666-z

Keywords

Search

Navigation