Abstract
Rapid industrialization, transportation and other human activities increase the formation of Ozone (O3) in the troposphere, causing an adverse effect on agricultural productivity. It is expected that concentration of O3 will increase along with the rise in global surface temperature. A field experiment was performed with differentially heat sensitive tomato (Solanum lycopersicum L.) cultivars with an objective to understand the intraspecific variations in defense mechanism under elevated O3 treatment. The selected tomato cultivars were exposed to ambient and elevated O3 (ambient ± 20 ppb) in open top chambers. The results depicted that elevated O3 induced accumulation of reactive oxygen species and malondialdehyde content leading to enhanced lipid peroxidation in all the tomato cultivars, but the scale of effects varied among cultivars. In response to oxidative stress generated due to ROS under elevated O3, activities of enzymatic and non-enzymatic antioxidants showed variable responses in differentially heat sensitive tomato cultivars. Heat tolerant cultivar, Superbug experienced highest oxidative stress under elevated O3, and significantly enhanced the non-enzymatic antioxidants leading to highest reduction in fruit biomass and total fresh fruit weight. However, heat tolerant cultivar, Kashi chayan and VRT 02 with lesser oxidative stress exhibited greater induction of enzymatic antioxidants and showed less reduction in fruit biomass and total fresh fruit weight. The heat sensitive cultivars, however, were less sensitive than Superbug. This study manifested that cultivar’s sensitivity under elevated O3 was governed by the variability of defense strategies, irrespective of their sensitivity towards heat. Kashi chayan and VRT 02 may be recommended in areas under elevated O3 to minimize the productivity losses.
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References
Abei H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ainsworth E, Yendrek C, Sitch S et al (2012) The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 63:637–661. https://doi.org/10.1146/annurev-arplant-042110-103829
Alexieva 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. https://doi.org/10.1046/J.1365-3040.2001.00778.X
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Booker FL, Burkey KO, Jones AM (2012) Re-evaluating the role of ascorbic acid and phenolic glycosides in ozone scavenging in the leaf apoplast of Arabidopsis thaliana L. Plant Cell Environ 35:1456–1466. https://doi.org/10.1111/J.1365-3040.2012.02502.X
Bray HG, Thorpe WV (1954) Analysis of phenolic compounds of interest in metabolism. Methods Biochem Anal 1:27–52. https://doi.org/10.1002/9780470110171.CH2
Camejo D, Jiménez A, Alarcón JJ et al (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct Plant Biol 33:177–187. https://doi.org/10.1071/FP05067
Caregnato FF, Bortolin RC, Divan Junior AM, Moreira JCF (2013) Exposure to elevated ozone levels differentially affects the antioxidant capacity and the redox homeostasis of two subtropical Phaseolus vulgaris L. varieties. Chemosphere 93:320–330. https://doi.org/10.1016/J.CHEMOSPHERE.2013.04.084
Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: From O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469. https://doi.org/10.1016/J.ENVPOL.2008.09.029
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chaudhary N, Agrawal SB (2015) The role of elevated ozone on growth, yield and seed quality amongst six cultivars of mung bean. Ecotoxicol Environ Saf 111:286–294. https://doi.org/10.1016/J.ECOENV.2014.09.018
Chaudhary I, Rathore D (2021) Assessment of ozone toxicity on cotton (Gossypium hirsutum L.) cultivars: Its defensive system and intraspecific sensitivity. Plant Physiol Biochem 166:912–927
Dalton DA, Russell SA, Hanus FJ et al (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci 83:3811–3815. https://doi.org/10.1073/PNAS.83.11.3811
Di Ferdinando M, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. In: Ahmad P, Prasad M (eds) Abiotic stress responses in plants. Springer, New York, pp. 159–179. https://doi.org/10.1007/978-1-4614-0634-1_9
Eghdami H, Werner W, Büker P, Sicard P (2022) Assessment of ozone risk to Central European forests: Time series indicates perennial exceedance of ozone critical levels. Environ Res 203:111798. https://doi.org/10.1016/j.envres.2021.111798
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal Biochem 70:616–620. https://doi.org/10.1016/0003-2697(76)90488-7
Fahey RC, Brown WC, Adams WB, Worsham MB (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129. https://doi.org/10.1128/JB.133.3.1126-1129.1978
Fatima A, Singh AA, Mukherjee A et al (2018) Variability in defence mechanism operating in three wheat cultivars having different levels of sensitivity against elevated ozone. Environ Exp Bot 155:66–78. https://doi.org/10.1016/j.envexpbot.2018.06.015
Feng Z, Kobayashi K (2009) Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis. Atmos Environ 43:1510–1519. https://doi.org/10.1016/J.ATMOSENV.2008.11.033
Feng Z, Xu Y, Kobayashi K et al (2022) Ozone pollution threatens the production of major staple crops in East Asia. Nat Food 31(3):47–56. https://doi.org/10.1038/s43016-021-00422-6
Flint SD, Jordan PW, Caldwell MM (1985) Plant protective response to enhanced UV-B radiation under field conditions: leaf optical properties and photosynthesis. Photochem Photobiol 41:95–99. https://doi.org/10.1111/J.1751-1097.1985.TB03454.X
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/PP.110.167569
Frahry G, Schopfer P (2001) NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 2122(212):175–183. https://doi.org/10.1007/S004250000376
Gallie DR (2013) The role of l-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443. https://doi.org/10.1093/JXB/ERS330
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/J.PLAPHY.2010.08.016
Gitelson AA, Merzlyak MN, Chivkunova OB (2001) Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochem Photobiol 74:38–45. https://doi.org/10.1562/0031-8655(2001)0740038OPANEO2.0.CO2
Griffiths PT, Murray LT, Zeng G et al (2021) Tropospheric ozone in CMIP6 simulations. Atmos Chem Phys 21:4187–4218. https://doi.org/10.5194/ACP-21-4187-2021
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. https://doi.org/10.1016/J.PLANTSCI.2004.07.027
Guo H, Sun Y, Yan H et al (2020) O3-induced priming defense associated with the abscisic acid signaling pathway enhances plant resistance to Bemisia tabaci. Front Plant Sci 11:93. https://doi.org/10.3389/FPLS.2020.00093/FULL
Gupta A, Yadav DS, Agrawal SB, Agrawal M (2022) Sensitivity of agricultural crops to tropospheric ozone : a review of Indian researches. Environ Monit Assess 194:894. https://doi.org/10.1007/s10661-022-10526-6
Halliwell B, Gutteridge JMC (1981) Formation of a thiobarbituric-acid-reactive substance from deoxyribose in the presence of iron salts. The role of superoxide and hydroxyl radicals. FEBS Lett 128(2):347–352
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Kapoor D, Sharma R, Handa N et al (2015) Redox homeostasis in plants under abiotic stress: Role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:13. https://doi.org/10.3389/FENVS.2015.00013/BIBTEX
Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J for Pathol 7:338–350. https://doi.org/10.1111/J.1439-0329.1977.TB00603.X
Kong JM, Chia LS, Goh NK et al (2003) Analysis and biological activities of anthocyanins. Phytochemistry 64:923–933. https://doi.org/10.1016/S0031-9422(03)00438-2
Kumari S, Lakhani A, Kumari KM (2020) First observation-based study on surface O3 trend in Indo-Gangetic Plain: Assessment of its impact on crop yield. Chemosphere 255:126972. https://doi.org/10.1016/J.CHEMOSPHERE.2020.126972
Laxman RH, Rao NKS, Biradar G et al (2014) Antioxidant enzymes activity and physiological response of tomato (Lycopersicon esculentum M.) genotypes under mild temperature stress. Indian J Plant Physiol 19:161–164. https://doi.org/10.1007/S40502-014-0091-X/TABLES/1
Lin D, Xiao M, Zhao J et al (2016) An overview of plant phenolic compounds and their importance in human nutrition and management of type 2 diabetes. Mol 21:1374. https://doi.org/10.3390/MOLECULES21101374
Liu Y, Tikunov Y, Schouten RE et al (2018) Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: A review. Front Chem 6:52. https://doi.org/10.3389/FCHEM.2018.00052/BIBTEX
Mills G, Buse A, Gimeno B et al (2007) A synthesis of AOT40-based response functions and critical levels of ozone for agricultural and horticultural crops. Atmos Environ 41:2630–2643
Mills G, Sharps K, Simpson D et al (2018) Ozone pollution will compromise efforts to increase global wheat production. Glob Chang Biol 24:3560–3574. https://doi.org/10.1111/gcb.14157
Mina U, Kumar P, Varshney C (2010) Effect of ozone exposure on growth, yield and isoprene emission from tomato (Lycopersicon esculentum L.) plants. Veg Crop Res Bull 72:35–48. https://doi.org/10.2478/v10032-010-0004-0
Mukherjee A, Singh Yadav D, Agrawal SB, Agrawal M (2020) Ozone a persistent challenge to food security in India: Current status and policy implications. Curr Opin Environ Sci Heal 19:100220. https://doi.org/10.1016/j.coesh.2020.10.008
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/OXFORDJOURNALS.PCP.A076232
Nimse SB, Pal D (2015) Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv 5:27986–28006. https://doi.org/10.1039/C4RA13315C
Oksanen E, Pandey V, Pandey AK et al (2013) Impacts of increasing ozone on Indian plants. Environ Pollut 177:189–200. https://doi.org/10.1016/J.ENVPOL.2013.02.010
Pandey A, Jaiswal D, Agrawal SB (2021) Ultraviolet-B mediated biochemical and metabolic responses of a medicinal plant Adhatoda vasica Nees. at different growth stages. J Photochem Photobiol B Biol. https://doi.org/10.1016/J.JPHOTOBIOL.2021.112142
Pellegrini E, Campanella A, Cotrozzi L et al (2017) What about the detoxification mechanisms underlying ozone sensitivity in Liriodendron tulipifera? Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-8818-7
Rahman SML, Nawata E, Domae Y, Sakuratani T (2000) Effects of water stress and temperature on sod activity, growth and yield of tomato. Acta Hortic 516:41–47
Ramya A, Dhevagi P, Priyatharshini S et al (2021) Response of rice (Oryza sativa L.) cultivars to elevated ozone stress. Environ Monit Assess 193:1–18. https://doi.org/10.1007/S10661-021-09595-W/FIGURES/10
Rathore D, Chaudhary IJ (2021) Effects of tropospheric ozone on groundnut (Arachis hypogea L.) cultivars: Role of plant age and antioxidative potential. Atmos Pollut Res 12:381–395. https://doi.org/10.1016/J.APR.2021.01.005
Ren Q, Sun Y, Guo H et al (2015) Elevated ozone induces jasmonic acid defense of tomato plants and reduces midgut proteinase activity in Helicoverpa armigera. Entomol Exp Appl 154:188–198. https://doi.org/10.1111/eea.12269
Sesso HD, Liu S, Gaziano JM, Buring JE (2003) Dietary lycopene, tomato-based food products and cardiovascular disease in women. J Nutr 133:2336–2341. https://doi.org/10.1093/JN/133.7.2336
Singh AA, Agrawal SB (2017) Tropospheric ozone pollution in India: effects on crop yield and product quality. Environ Sci Pollut Res 24:4367–4382. https://doi.org/10.1007/s11356-016-8178-8
Solomon S, Martin M, Melinda M, Dahe Q (2007) Climate Change 2007-the Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC. Cambridge university press
Stevenson D, Doherty R, Sanderson M et al (2005) Impacts of climate change and variability on tropospheric ozone and its precursors. Faraday Discuss 130:41–57. https://doi.org/10.1039/B417412G
Subba Rao PV, Towers GHN (1970) L-phenylalanine ammonia-lyase (Ustilago bordei). Methods Enzymol 17:581–585. https://doi.org/10.1016/0076-6879(71)17244-8
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant J 11:1187–1194. https://doi.org/10.1046/J.1365-313X.1997.11061187.X
Wang J, Zeng Q, Zhu J et al (2013) Dissimilarity of ascorbate–glutathione (AsA–GSH) cycle mechanism in two rice (Oryza sativa L.) cultivars under experimental free-air ozone exposure. Agric Ecosyst Environ 165:39–49. https://doi.org/10.1016/J.AGEE.2012.12.006
Wohlgemuth H, Mittelstrass K, Kschieschan S et al (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. https://doi.org/10.1046/J.1365-3040.2002.00859.X
Xu C, Natarajan S, Sullivan JH (2008) Impact of solar ultraviolet-B radiation on the antioxidant defense system in soybean lines differing in flavonoid contents. Environ Exp Bot 63:39–48. https://doi.org/10.1016/J.ENVEXPBOT.2007.10.029
Yadav DS, Rai R, Mishra AK et al (2019) ROS production and its detoxification in early and late sown cultivars of wheat under future O3 concentration. Sci Total Environ 659:200–210. https://doi.org/10.1016/j.scitotenv.2018.12.352
Yadav DS, Agrawal SB, Agrawal M (2021) Ozone flux-effect relationship for early and late sown Indian wheat cultivars : Growth, biomass, and yield. F Crop Res 263:108076. https://doi.org/10.1016/j.fcr.2021.108076
You J, Chan Z (2015) Ros regulation during abiotic stress responses in crop plants. Front Plant Sci 6:1092. https://doi.org/10.3389/FPLS.2015.01092/BIBTEX
Acknowledgements
The authors are thankful to the Head, Department of Botany, and the Co-ordinator, Institute of Eminence and Interdisciplinary School of Life Sciences, Banaras Hindu University for providing all the laboratory facilities. We are also thankful to Dr. Nagendra Rai [Principle Scientist, ICAR-IIVR (Indian Institute of Vegetable Research), Varanasi] for providing seeds of tomato cultivars. University Grants Commission (UGC), New Delhi, India is greatly acknowledged for providing the financial support in the form of Senior Research Fellowship to Akanksha Gupta. Madhoolika Agrawal is also thankful to SERB, New Delhi for providing J.C. Bose Fellowship.
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This work was supported by University Grants Commission (UGC), New Delhi, India, for providing financial support in the form of UGC-JRF-SRF (UGC- Ref.No.: 1042/ CSIR-UGC NET JUNE 2019).
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Akanksha Gupta: Conceptualization, Data curation, Interpretation, Visualization, Writing original draft. Shashi Bhushan Agrawal: Visualization, Writing-Review & Editing. Madhoolika Agrawal: Validation, Writing—Review & Editing and Supervision. All authors read and approved the final manuscript.
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Gupta, A., Agrawal, S.B. & Agrawal, M. Evaluation of Toxicity of Tropospheric Ozone on Tomato (Solanum lycopersicum L.) Cultivars: ROS Production, Defense Strategies and Intraspecific Sensitivity. J Plant Growth Regul 42, 6444–6460 (2023). https://doi.org/10.1007/s00344-022-10870-4
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DOI: https://doi.org/10.1007/s00344-022-10870-4