Protoplasma

, Volume 252, Issue 3, pp 797–811 | Cite as

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

Original Article
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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.

Keywords

OTCs O3 Vigna radiata L Injury Physiology Protein profile 
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Notes

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.

References

  1. 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 10:2605–2619CrossRefPubMedGoogle Scholar
  2. Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci India 82:1227–1238Google Scholar
  3. Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 28:949–964CrossRefGoogle Scholar
  4. 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 100:114–121CrossRefGoogle Scholar
  5. 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 72:248–254CrossRefPubMedGoogle Scholar
  6. 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 27–52CrossRefGoogle Scholar
  7. 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 199:275–285CrossRefGoogle Scholar
  8. Burkey KO, Eason G, Fiscus EL (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiol Plant 117:51–57CrossRefGoogle Scholar
  9. Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42:549–555CrossRefPubMedGoogle Scholar
  10. Calatayud V, Cervero J, Sanz MJ (2007) Foliar, physiological and growth responses of four maple species exposed to ozone. Water Air Soil Pollut 185:239–254CrossRefGoogle Scholar
  11. Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469CrossRefPubMedGoogle Scholar
  12. Castagna A, Nali C, Ciompi S, Lorenzini G, Soldatini GF, Raineri A (2001) Ozone exposure effects photosynthesis of pumpkin (Cucurbita pepo) plants. New Phytol 152:223–229CrossRefGoogle Scholar
  13. Chang YS, Yu MR (2001) Correlation between ozone resistance and relative chlorophyll fluorescence or relative stomatal conductance of bedding plants. Bot Bull Acad Sin 42:265–272Google Scholar
  14. 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):5318–5329CrossRefGoogle Scholar
  15. 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):7793–7807CrossRefPubMedGoogle Scholar
  16. Debaje SB, Kakade AD, Jeyakumar SJ (2010) Air pollution effect of O3 on crop yield in rural area. J Hazard Mater 183:773–779CrossRefPubMedGoogle Scholar
  17. 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 111:789–796PubMedCentralPubMedGoogle Scholar
  18. 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 28:1761–1772CrossRefPubMedGoogle Scholar
  19. Duxbury AC, Yentsch CS (1956) Plankton pigment monographs. J Mar Res 15:19–101Google Scholar
  20. Faoro F, Iriti M (2009) Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. Environ Pollut 157:1470–1477CrossRefPubMedGoogle Scholar
  21. 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 14:2696–2708Google Scholar
  22. Fiscus EL, Booker FL, Burkey KO (2005) Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant Cell Environ 28(8):997–1011CrossRefGoogle Scholar
  23. Fuhrer J, Booker FL (2003) Ecological issues related to ozone: agricultural issues. Environ Int 29:141–154CrossRefPubMedGoogle Scholar
  24. Fuhrer J, Skarby L, Ashmore MR (1997) Critical levels for ozone effects on vegetation in Europe. Environ Pollut 97:91–106CrossRefPubMedGoogle Scholar
  25. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:900–930CrossRefGoogle Scholar
  26. 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 154:167–172CrossRefGoogle Scholar
  27. 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 156:377–388CrossRefGoogle Scholar
  28. 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 168:153–160CrossRefGoogle Scholar
  29. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, OxfordGoogle Scholar
  30. Heath RL (2008) Modification of the biochemical pathways of plants induced by ozone: what are the varied route to changes? Environ Pollut 155:453–463CrossRefPubMedGoogle Scholar
  31. Iriti M, Faoro F (2008) Oxidative stress, the paradigm of ozone toxicity in plants and animals. Water Air Soil Pollut 187:285–301CrossRefGoogle Scholar
  32. Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44CrossRefGoogle Scholar
  33. Kangasjarvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–1036CrossRefGoogle Scholar
  34. Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J For Pathol 7:338–350CrossRefGoogle Scholar
  35. Kley D, Kleinmann M, Sanderman H, Krupa S (1999) Photochemical oxidants: state of the science. Environ Pollut 100:19–42CrossRefPubMedGoogle Scholar
  36. 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 101:146–156CrossRefGoogle Scholar
  37. Langebartels C, Wohlgemuth H, Kschieschan S (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40:567–575CrossRefGoogle Scholar
  38. 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 69–88Google Scholar
  39. Maclachalan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of chlorophyll mutant barley. Can J Bot 41:1053–1063CrossRefGoogle Scholar
  40. 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 26:237–287CrossRefGoogle Scholar
  41. 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 87:197–205CrossRefPubMedGoogle Scholar
  42. 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 200:273–289CrossRefGoogle Scholar
  43. 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 145:21–32CrossRefGoogle Scholar
  44. 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):139–149PubMedGoogle Scholar
  45. 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 24:327–336CrossRefGoogle Scholar
  46. 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 138:295–305CrossRefGoogle Scholar
  47. Pacifici RE, Davis KJA (1990) Protein degradation as an index of oxidative stress. Methods Enzymol 186:485–502CrossRefPubMedGoogle Scholar
  48. 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 193:1–5CrossRefPubMedGoogle Scholar
  49. Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone induced oxidative stress: mechanism of action and reaction. Physiol Plant 100:264–273CrossRefGoogle Scholar
  50. 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 135:310–317CrossRefGoogle Scholar
  51. 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 407:679–691CrossRefPubMedGoogle Scholar
  52. 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 352–357Google Scholar
  53. 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 154:250–255CrossRefGoogle Scholar
  54. 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 109:421–432PubMedCentralPubMedGoogle Scholar
  55. Saitanis CJ, Riga-Karandinos AN, Karandinos MG (2001) Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere 42:945–953CrossRefPubMedGoogle Scholar
  56. 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 216:918–928PubMedGoogle Scholar
  57. 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–S24CrossRefGoogle Scholar
  58. 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 57:89–97CrossRefGoogle Scholar
  59. 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 4:44–48CrossRefGoogle Scholar
  60. 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):2399–2411CrossRefGoogle Scholar
  61. 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 135:168–177CrossRefGoogle Scholar
  62. 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 21:2628–2641CrossRefGoogle Scholar
  63. 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 581Google Scholar
  64. Sun J, Feng Z, Ort DR (2014) Impacts of rising tropospheric ozone on photosynthesis and metabolite levels on field grown soybean. Plant Sci 226:147–161CrossRefPubMedGoogle Scholar
  65. Tiwari S, Rai R, Agrawal M (2008) Annual and seasonal variations in tropospheric ozone concentrations around Varanasi. Int J Remote Sens 29:4499–4514CrossRefGoogle Scholar
  66. 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 85:1–12CrossRefGoogle Scholar
  67. 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, 2008Google Scholar
  68. 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 43:604–618CrossRefGoogle Scholar
  69. Vingarzan R (2004) A review of surface ozone background levels and trends. Atmos Environ 38:3431–3442CrossRefGoogle Scholar
  70. Wahid A (2006) Productivity losses in barley attributable to ambient atmospheric pollutants in Pakistan. Atmos Environ 40:5342–5354CrossRefGoogle Scholar
  71. 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 30:1150–1162CrossRefPubMedGoogle Scholar
  72. 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 25:717–726CrossRefGoogle Scholar
  73. 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 38:403–411CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Laboratory of Air Pollution and Global Climate Change, Department of BotanyBanaras Hindu UniversityVaranasiIndia

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