Skip to main content
SpringerLink
Log in

Biochemical and physiological characteristics of tropical mung bean (Vigna radiata L.) cultivars against chronic ozone stress: an insight to cultivar-specific response

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Surface-level ozone (O3) has been regarded as one of the most significant phytotoxic pollutants worldwide. Investigations addressing adverse impacts of elevated O3 on mung bean (Vigna radiata L.), an important leguminous crop of the Indian subcontinent, are still limited. The present study analyzed the differences on the foliar injury, reactive oxygen species (ROS) generation, antioxidative defense system, physiology, and foliar protein profile of two tropical mung bean cultivars (HUM-2 and HUM-6) exposed to elevated O3 under near-natural conditions. Both cultivars were negatively affected by the pollutant, but the response was cultivar-specific. Results revealed that elevated O3 induced higher levels of ROS (O2 ·− and H2O2) and lipid peroxidation leading to greater foliar injury in HUM-2 compared to HUM-6. Photosynthetic pigments, photosynthetic rate, stomatal conductance, and photochemical efficiency reduced under elevated O3 exposure and the extent of reduction was higher in HUM-2. Principal component analysis revealed that photosynthetic performance and quantum yield were drastically affected in HUM-2 as compared to HUM-6. Activities of antioxidative enzymes were also stimulated, suggesting generation of oxidative stress under elevated O3. HUM-6 showed higher induction of antioxidative enzymes than HUM-2. One-dimensional gel electrophoresis analysis showed drastic reductions in the abundantly present ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) large and small subunits and the decrease was higher in HUM-2. Altogether, results suggested that higher accumulation of ROS and limited induction of antioxidant defense system led to more leaf injury and impairment of photosynthesis in HUM-2 than HUM-6 depicting its higher sensitivity towards elevated O3.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahsan N, Nanjo Y, Sawada H, Kohno Y, Komatsu S (2010) Ozone stress induced proteomic changes in leaf total soluble and chloroplast proteins of soybean reveal that carbon allocation is involved in adaptation in the early developmental stage. Proteomics 10:2605–2619

    Article  CAS  PubMed  Google Scholar 

  • Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci India 82:1227–1238

    CAS  Google Scholar 

  • Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 28:949–964

    Article  CAS  Google Scholar 

  • Bortolin RC, Caregnato FF, Divan AM Jr, Reginatto FH, Gelain DP, Moreira JC (2014) Effects of chronic elevated ozone concentration on the redox state and fruit yield of red pepper plant Capsicum baccatum. Ecotoxicol Environ Safe 100:114–121

    Article  CAS  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 WV (1954) Analysis of phenolic compounds of interest in metabolism. In: Glick D (ed) Methods of biochemical analysis. Interscience, New York, pp 27–52

    Chapter  Google Scholar 

  • Burkart S, Bender J, Tarkotta B, Faust S, Castagna A, Ranieri A, Weigel HJ (2013) Effects of ozone on leaf senescence, photochemical efficiency and grain yield in two winter wheat cultivars. J Agron Crop Sci 199:275–285

    Article  CAS  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 

  • Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42:549–555

    Article  CAS  PubMed  Google Scholar 

  • Calatayud V, Cervero J, Sanz MJ (2007) Foliar, physiological and growth responses of four maple species exposed to ozone. Water Air Soil Pollut 185:239–254

    Article  CAS  Google Scholar 

  • Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469

    Article  CAS  PubMed  Google Scholar 

  • Castagna A, Nali C, Ciompi S, Lorenzini G, Soldatini GF, Raineri A (2001) Ozone exposure effects photosynthesis of pumpkin (Cucurbita pepo) plants. New Phytol 152:223–229

    Article  CAS  Google Scholar 

  • Chang YS, Yu MR (2001) Correlation between ozone resistance and relative chlorophyll fluorescence or relative stomatal conductance of bedding plants. Bot Bull Acad Sin 42:265–272

    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(8):5318–5329

    Article  CAS  Google Scholar 

  • Chaudhary N, Singh S, Agrawal SB, Agrawal M (2013) Assessment of six Indian cultivars of mung bean against ozone by using foliar injury index and changes in carbon assimilation, gas exchange, chlorophyll fluorescence and photosynthetic pigments. Environ Monit Assess 185(9):7793–7807

    Article  CAS  PubMed  Google Scholar 

  • Debaje SB, Kakade AD, Jeyakumar SJ (2010) Air pollution effect of O3 on crop yield in rural area. J Hazard Mater 183:773–779

    Article  CAS  PubMed  Google Scholar 

  • Desimone M, Henke A, Wagner E (1996) Oxidative stress induced partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111:789–796

    PubMed Central  CAS  PubMed  Google Scholar 

  • Di Baccio D, Castagna A, Paoletti E, Sebastiani L, Ranieri A (2008) Could the differences in O3 sensitivity between two poplar clones be related to a difference in antioxidant defense and secondary metabolic response to O3 influx? Tree Physiol 28:1761–1772

    Article  PubMed  Google Scholar 

  • Duxbury AC, Yentsch CS (1956) Plankton pigment monographs. J Mar Res 15:19–101

    Google Scholar 

  • Faoro F, Iriti M (2009) Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. Environ Pollut 157:1470–1477

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Kobayashi K, Ainsworth EA (2008) Impact of elevated ozone concentration on growth, physiology and yield of wheat (Triticum aestivum L.): a meta-analysis. Glob Chang Biol 14:2696–2708

    Google Scholar 

  • Fiscus EL, Booker FL, Burkey KO (2005) Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant Cell Environ 28(8):997–1011

    Article  CAS  Google Scholar 

  • Fuhrer J, Booker FL (2003) Ecological issues related to ozone: agricultural issues. Environ Int 29:141–154

    Article  CAS  PubMed  Google Scholar 

  • Fuhrer J, Skarby L, Ashmore MR (1997) Critical levels for ozone effects on vegetation in Europe. Environ Pollut 97:91–106

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:900–930

    Article  Google Scholar 

  • Guidi L, Bongi G, Ciompi S, Soldatini GF (1999) In Vicia faba leaves photoinhibition from ozone fumigation in light precedes a decrease in quantum yield of functional PSII centres. J Plant Physiol 154:167–172

    Article  CAS  Google Scholar 

  • Guidi L, Degl’Innocenti E, Soldatini GF (2002) Assimilation of CO2, enzyme activation and photosynthetic electron transport in bean leaves, as affected by high light and ozone. New Phytol 156:377–388

    Article  CAS  Google Scholar 

  • Guidi L, Degl’Innocenti E, Genovesi S, Soldatini GF (2005) Photosynthetic process and activities of enzymes involved in the phenylpropanoid pathway in resistant and sensitive genotypes of Lycopersicon esculentum L. exposed to ozone. Plant Sci 168:153–160

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • Heath RL (2008) Modification of the biochemical pathways of plants induced by ozone: what are the varied route to changes? Environ Pollut 155:453–463

    Article  CAS  PubMed  Google Scholar 

  • Iriti M, Faoro F (2008) Oxidative stress, the paradigm of ozone toxicity in plants and animals. Water Air Soil Pollut 187:285–301

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kangasjarvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–1036

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kley D, Kleinmann M, Sanderman H, Krupa S (1999) Photochemical oxidants: state of the science. Environ Pollut 100:19–42

    Article  CAS  PubMed  Google Scholar 

  • Kumari S, Agrawal M (2014) Growth, yield and quality attributes of a tropical potato variety (Solanum tuberosum L. cv Kufri chandramukhi) under ambient and elevated carbon dioxide and ozone and their interactions. Ecotoxicol Environ Safe 101:146–156

    Article  CAS  Google Scholar 

  • Langebartels C, Wohlgemuth H, Kschieschan S (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40:567–575

    Article  CAS  Google Scholar 

  • Long SP, Naidu SL (2002) Effects of oxidants at the biochemical, cell and physiological levels, with particular reference to ozone. In: Bell JNB, Treshow M (eds) Air pollution and plant life, 2nd edn. Wiley, UK, pp 69–88

    Google Scholar 

  • Maclachalan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of chlorophyll mutant barley. Can J Bot 41:1053–1063

    Article  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. Annu Rev Energy Environ 26:237–287

    Article  Google Scholar 

  • Mikkelsen TN, Dodell B, Lutz C (1995) Changes in pigment concentration and composition of Norway spruce induced by long-term exposure to low levels of ozone. Environ Pollut 87:197–205

    Article  CAS  PubMed  Google Scholar 

  • Mishra AK, Agrawal SB (2014) Cultivar specific response of CO2 fertilization on two tropical mung bean (Vigna radiata L.) cultivars: ROS generation, antioxidant status, physiology, growth, yield and seed quality. J Agron Crop Sci 200:273–289

    Article  CAS  Google Scholar 

  • Mishra AK, Rai R, Agrawal SB (2013a) Differential response of dwarf and tall tropical wheat cultivars to elevated ozone with and without carbon dioxide enrichment: growth, yield and grain quality. Field Crop Res 145:21–32

    Article  Google Scholar 

  • Mishra AK, Rai R, Agrawal SB (2013b) Individual and interactive effects of elevated carbon dioxide and ozone on tropical wheat (Triticum aestivum L.) with special emphasis on ROS generation and activation of antioxidant defence system. Indian J Biochem Biophys 50(2):139–149

    CAS  PubMed  Google Scholar 

  • Noormets A, Sôber A, Pell EJ, Dickson RE, Podila GK, Sôber J, Isebrands JG, Karnosky DF (2001) Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/or O3. Plant Cell Environ 24:327–336

    Article  CAS  Google Scholar 

  • Paakkonen E, Seppanen S, Holopainen T, Kokko H, Karenlampi S, Karenlampi L, Kangasjarvi J (1998) Induction of genes for the stress proteins PR-10 and PAL in relation to growth, visible injuries and stomatal conductance in birch (Betula pendula) clones exposed to ozone and/or drought. New Phytol 138:295–305

    Article  CAS  Google Scholar 

  • Pacifici RE, Davis KJA (1990) Protein degradation as an index of oxidative stress. Methods Enzymol 186:485–502

    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 

  • Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone induced oxidative stress: mechanism of action and reaction. Physiol Plant 100:264–273

    Article  CAS  Google Scholar 

  • Picchi V, Iriti M, Quaroni S, Saracchi M, Viola P, Faoro F (2010) Climatic variations and phonological stages modulate ozone damages in field-grown wheat. A three-year study with eight modern cultivars in Po Valley (Northern Italy). Agric Ecosyst Environ 135:310–317

    Article  CAS  Google Scholar 

  • Rai R, Agrawal M (2008) Evaluation of physiological and biochemical responses of two rice (Oryza sativa L.) cultivars to ambient air pollution using open top chambers at a rural site in India. Sci Total Environ 407:679–691

    Article  CAS  PubMed  Google Scholar 

  • Ranieri A, Nali C, Amoroso S, Lorenzini G, Soldatini GF (1996) Are peroxidase systems related to different ozone resistence of poplar clones? In: Obinger C, Burner U, Ebermann R, Penel C, Greppin H (ed), Plant Peroxidases: Biochemistry and Physiology. University of Geneva, pp 352–357

  • Ranieri A, Castagna A, Padu E, Moldau H, Rahi M, Soldatini GF (1999) The decay of O3 through direct reaction with cell wall ascorbate is not sufficient to explain the different degrees of O3 sensitivity in two poplar clones. J Plant Physiol 154:250–255

    Article  CAS  Google Scholar 

  • Rao MV, Hale BA, Ormrod DP (1995) Amelioration of ozone induced oxidative damage in wheat plants grown under high carbon dioxide (role of antioxidant enzymes). Plant Physiol 109:421–432

    PubMed Central  CAS  PubMed  Google Scholar 

  • Saitanis CJ, Riga-Karandinos AN, Karandinos MG (2001) Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere 42:945–953

    Article  CAS  PubMed  Google Scholar 

  • Sanmartin M, Drogoudi PD, Pateraki TLI, Barnes J, Kanellis AK (2003) Overexpression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216:918–928

    CAS  PubMed  Google Scholar 

  • Sarkar A, Agrawal SB (2012) Evaluating the response of two high yielding Indian rice cultivars against ambient and elevated levels of ozone by using open top chambers. J Environ Manag 95:S19–S24

    Article  CAS  Google Scholar 

  • Scebba F, Giuntini D, Castagna A, Soldatini G, Ranieri A (2006) Analysing the impact of ozone on biochemical and physiological variables in plant species belonging to natural ecosystems. Environ Exp Bot 57:89–97

    Article  CAS  Google Scholar 

  • Serengil Y, Augustaitis A, Bytnerowicz A, Grulke N, Kozovitz AR, Matyssek R, Müller-Starck G, Schaub M, Wieser G, Coskun AA, Paoletti E (2011) Adaptation of forest ecosystems to air pollution and climate change: a global assessment on research priorities. iForest-Biogeosci For 4:44–48

    Article  Google Scholar 

  • Singh S, Agrawal SB (2011) Ambient ozone and two black gram cultivars: an assessment of amelioration by the use of ethylenediurea. Acta Physiol Plant 33(6):2399–2411

    Article  CAS  Google Scholar 

  • Singh E, Tiwari S, Agrawal M (2010) Variability in antioxidant and metabolite levels, growth and yield of two soybean varieties: An assessment of anticipated yield losses under projected elevation of ozone. Agric Ecosyst Environ 135:168–177

    Article  CAS  Google Scholar 

  • Singh AA, Agrawal SB, Shahi JP, Agrawal M (2014) 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 

  • Subba Rao PV, Tower GHN (1970) L-phenylalanine ammonia-lyase (Ustilago hordei). In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic, New York, p 581

    Google Scholar 

  • Sun J, Feng Z, Ort DR (2014) Impacts of rising tropospheric ozone on photosynthesis and metabolite levels on field grown soybean. Plant Sci 226:147–161

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Rai R, Agrawal M (2008) Annual and seasonal variations in tropospheric ozone concentrations around Varanasi. Int J Remote Sens 29:4499–4514

    Article  Google Scholar 

  • Tripathi R, Agrawal SB (2012) Effects of ambient and elevated level of ozone on Brassica campestris L. with special reference to yield and oil quality parameters. Ecotoxicol Environ Safe 85:1–12

    Article  CAS  Google Scholar 

  • UNECE (2008) Review of the 1999 Gothenburg Protocol. Report by the Secretariat. UNECE executive body for the convention on long-range transboundary air pollution. ECE/ EB.AIR/2007/10, 2008

  • Van Dingenen R, Dentener FJ, Raes F, Krol 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 

  • Vingarzan R (2004) A review of surface ozone background levels and trends. Atmos Environ 38:3431–3442

    Article  CAS  Google Scholar 

  • Wahid A (2006) Productivity losses in barley attributable to ambient atmospheric pollutants in Pakistan. Atmos Environ 40:5342–5354

    Article  CAS  Google Scholar 

  • Wittig VE, Ainsworth EA, Long SP (2007) To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. Plant Cell Environ 30:1150–1162

    Article  CAS  PubMed  Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel HJ, Overmyer K, Kangasjarvi J, Langebartels C, Sandermann H (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ 25:717–726

    Article  CAS  Google Scholar 

  • Zheng Y, Lyons T, Ollerenshaw JH, Barnes JD (2000) Ascorbate in the leaf apoplast is a factor mediating ozone resistance in Plantago major. Plant Physiol Biochem 38:403–411

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Head and Coordinator, Center of Advanced Study, Department of Botany, Banaras Hindu University, Varanasi for providing necessary laboratory and field facilities and to Prof. M.N. Singh, Department of Genetics and Plant Breeding, Institute of Agricultural Sciences, Banaras Hindu University for providing mung bean seeds. Authors also want to extend thanks to Mr. Bhanu Pandey for providing help during PCA. Financial assistance in the form a research project (CST/D-1179) from Council of Science and Technology (CST), Lucknow, Uttar Pradesh is gratefully acknowledged. Amit Kumar Mishra is thankful to the Center of Advanced Study, Department of Botany for awarding Junior Research Fellowship. Special thanks are due to both the anonymous reviewers for their valuable suggestions and corrections for improving the quality of the manuscript.

Author information

Authors and Affiliations

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

    Amit Kumar Mishra & S. B. Agrawal

Authors
  1. Amit Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. B. Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. B. Agrawal.

Additional information

Handling Editor: Néstor Carrillo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, A.K., Agrawal, S.B. 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 (2015). https://doi.org/10.1007/s00709-014-0717-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-014-0717-x

Keywords

Search

Navigation