Role of antioxidant pool in management of ozone stress through soil nitrogen amendments in two cultivars of a tropical legume
Gereraj Sen Gupta A and Supriya Tiwari
A B
+ Author Affiliations
- Author Affiliations
A Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, India.
B Corresponding author. Email: supriyabhu@gmail.com
Functional Plant Biology - https://doi.org/10.1071/FP20159
Submitted: 7 June 2020 Accepted: 14 October 2020 Published online: 1 December 2020
Abstract
The present experiment was done on two different cultivars of a tropical legume, Cymopsis tetragonoloba L. Taub. (cluster bean) cvv. Pusa-Naubahar (PUSA-N) and Selection-151 (S-151). The experiment was conducted under ambient ozone (O3) conditions with inputs of three different doses of inorganic nitrogen (N1, recommended; N2, 1.5-times recommended and N3, 2-times recommended) as well as control plants. The objective of this study was to evaluate the effectiveness of soil nitrogen amendments in management of ambient ozone stress in the two cultivars of C. tetragonoloba. Our experiment showed that nitrogen amendments can be an efficient measure to manage O3 injury in plants. Stimulation of antioxidant enzyme activities under nitrogen amendments is an important feature of plants that help plants cope with ambient O3 stress. Nitrogen amendments strengthened the antioxidant machinery in a more effective way in the tolerant cultivar PUSA-N, while in the sensitive cultivar S-151, avoidance strategy marked by more reduction in stomatal conductance was more prominent. Enzymes of the Halliwell–Asada pathway, especially ascorbate peroxidase and glutathione reductase, were more responsive and synchronised in PUSA-N than S-151, under similar nitrogen amendment regimes and were responsible for the differential sensitivities of the two cultivars of C. tetragonoloba. The present study shows that 1.5-times recommended dose of soil nitrogen amendments was sufficient in partial mitigation of O3 injury and the higher nitrogen dose (2-times recommended, in our case), did not provide any extra advantage to the plant’s metabolism compared with plants treated with the lower nitrogen dose (1.5-times recommended).
Keywords: cluster bean, Cymopsis tetragonoloba L. Taub, enzymatic antioxidants, nitrogen amendments, non-enzymatic antioxidants, oxidative damage, ozone stress, partial mitigation.
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |
Agathokleous E (2017) Perspectives for elucidating the ethylene-diurea (EDU) mode of action for protection against O3 phytotoxicity. Ecotoxicology and Environmental Safety 142, 530–537.
| Perspectives for elucidating the ethylene-diurea (EDU) mode of action for protection against O3 phytotoxicity.Crossref | GoogleScholarGoogle Scholar | 28478379PubMed |
Agathokleous E, Saitanis CJ, Koike T (2015) Tropospheric O3, the nightmare of wild plants: a review study. Journal of Agricultural Meteorology 71, 142–152.
| Tropospheric O3, the nightmare of wild plants: a review study.Crossref | GoogleScholarGoogle Scholar |
Agathokleous E, Paoletti E, Saitanis CJ, Manning WJ, Sugai T, Koike T (2016) Impacts of ethylenediurea (EDU) soil drench and foliar spray in Salix sachalinensis protection against O3-induced injury. The Science of the Total Environment 573, 1053–1062.
| Impacts of ethylenediurea (EDU) soil drench and foliar spray in Salix sachalinensis protection against O3-induced injury.Crossref | GoogleScholarGoogle Scholar | 27607908PubMed |
Ainsworth EA (2017) Understanding and improving global crop response to ozone pollution. The Plant Journal 90, 886–897.
| Understanding and improving global crop response to ozone pollution.Crossref | GoogleScholarGoogle Scholar | 27739639PubMed |
Alexieva V, Sergiev I, Mapelli S, Karano E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell & Environment 24, 1337–1344.
| The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat.Crossref | GoogleScholarGoogle Scholar |
Anderson ME (1996) Glutathione. In ‘Free radicals: a practical approach’. (Eds NA Punchard and FJ Kelly) pp. 213–226. (Oxford University Press: Oxford)
Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances 27, 84–93.
| Biotechnological approach of improving plant salt tolerance using antioxidants as markers.Crossref | GoogleScholarGoogle Scholar | 18950697PubMed |
Bellini E, De Tullio MC (2019) Ascorbic acid and ozone: novel perspectives to explain an elusive relationship. Plants 8, 122
| Ascorbic acid and ozone: novel perspectives to explain an elusive relationship.Crossref | GoogleScholarGoogle Scholar |
Bielenberg DG, Lynch JP, Pell EJ (2002) Nitrogen dynamics during O3-induced accelerated senescence in hybrid poplar. Plant, Cell & Environment 25, 501–512.
| Nitrogen dynamics during O3-induced accelerated senescence in hybrid poplar.Crossref | GoogleScholarGoogle Scholar |
Bray HG, Thorpe WY (1954) Analysis of phenolic compounds of interest in metabolism. Methods of Biochemical Analysis 1, 27–52.
| Analysis of phenolic compounds of interest in metabolism.Crossref | GoogleScholarGoogle Scholar | 13193524PubMed |
Caregnato FF, Bortolin RF, Divan 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.
| Exposure to elevated ozone levels differentially affects the antioxidant capacity and the redox homeostasis of two subtropical Phaseolus vulgaris L. varieties.Crossref | GoogleScholarGoogle Scholar | 23714146PubMed |
Cooper OR, Parrish DD, Ziemke J, Balashov NV, Cupeiro M, Galbally IE, Gilge S, Horowitz L, Jensen NR, Lamarque JF, Naik V (2014) Global distribution and trends of tropospheric ozone: an observation-based review. Elementa: Science of the Anthropocene 2, p.000029
| Global distribution and trends of tropospheric ozone: an observation-based review.Crossref | GoogleScholarGoogle Scholar | 33249522PubMed |
Dai L, Feng Z, Pan X, Xu Y, Li P, Lefohn AS, Harmens H, Kobayashi K (2019) Increase of apoplastic ascorbate induced by ozone is insufficient to remove the negative effects in tobacco, soybean and poplar. Environmental Pollution 245, 380–388.
| Increase of apoplastic ascorbate induced by ozone is insufficient to remove the negative effects in tobacco, soybean and poplar.Crossref | GoogleScholarGoogle Scholar | 30448508PubMed |
Dizengremel P, Le Thiec D, Bagard M, Jolviet Y (2008) Ozone risk assessment for plants: central role of metabolism dependant changes in reducing power. Environmental Pollution 156, 11–15.
| Ozone risk assessment for plants: central role of metabolism dependant changes in reducing power.Crossref | GoogleScholarGoogle Scholar | 18243452PubMed |
Dumont J, Keski-Saari S, Keinänen M, Cohen D, Ningre N, Kontunen-Soppela S, Baldet P, Gibon Y, Dizengremel P, Vaultier MN, Jolivet Y, Oksanen E, Le Thiec D (2014) Ozone affects ascorbate and glutathione biosynthesis as well as amino acid contents in three Euramerican poplar genotypes. Tree Physiology 34, 253–266.
| Ozone affects ascorbate and glutathione biosynthesis as well as amino acid contents in three Euramerican poplar genotypes.Crossref | GoogleScholarGoogle Scholar | 24682617PubMed |
Duxbury AC, Yentsch CS (1956) Plankton pigment monographs. Journal of Marine Research 15, 19–101.
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium-chloride: a simple assay for superoxide dismutase. Analytical Biochemistry 70, 616–620.
| Inhibition of nitrite formation from hydroxylammonium-chloride: a simple assay for superoxide dismutase.Crossref | GoogleScholarGoogle Scholar | 817618PubMed |
Emberson L, Büker P (2008) Ozone: a threat to food security in South Asia. Policy brief. (Stockholm Environment Institute, University of York, UK.) Available at www.sei.se [Verified 20 October 2020].
Emberson LD, Pleijel H, Ainsworth EA, van den Berg M, Ren W, Osborne S (2018) Ozone effects on crops and consideration in crop models. European Journal of Agronomy 100, 19–34.
| Ozone effects on crops and consideration in crop models.Crossref | GoogleScholarGoogle Scholar |
Fatima A, Singh AA, Mukherjee A, Dolker T, Agrawal M, Agrawal SB (2019) Assessment of ozone sensitivity in three wheat cultivars using ethylenediurea. Plants 8, 80
| Assessment of ozone sensitivity in three wheat cultivars using ethylenediurea.Crossref | GoogleScholarGoogle Scholar |
Fowler D, Amann M, Anderson F, Ashmore M, Cox P, Depledge M, Derwent D, Grennfelt P, Hewitt N, Hov O, Jenkin M (2008) Ground-level ozone in the 21st century: future trends, impacts and policy implications. Royal Society Scientific Policy Report 15, 1–132.
Fridovich I (1974) Superoxide dismutase. Advances in Enzymology 41, 35–97.
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpi’nski S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiology 171, 1606–1615.
| ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants.Crossref | GoogleScholarGoogle Scholar | 27208294PubMed |
Guidi L, Nali C, Lorenzini G, Filppi F, Soladatini GF (2001) Effect of chronic ozone fumigation on the photosynthetic process of poplar clones showing different sensitivity. Environmental Pollution 113, 245–254.
| Effect of chronic ozone fumigation on the photosynthetic process of poplar clones showing different sensitivity.Crossref | GoogleScholarGoogle Scholar | 11428132PubMed |
Gupta SK, Sharma M, Majumder B, Maurya VK, Lohani M, Deeba F, Pandey V (2018) Impact of ethylene di-urea (EDU) on growth, yield and proteome of two winter wheat varieties under high ambient ozone phytotoxicity. Chemosphere 196, 161–173.
| Impact of ethylene di-urea (EDU) on growth, yield and proteome of two winter wheat varieties under high ambient ozone phytotoxicity.Crossref | GoogleScholarGoogle Scholar | 29304454PubMed |
Harmens H, Hayes F, Sharps K, Mills G, Calatayud V (2017) Leaf traits and photosynthetic responses of Betula pendula saplings to a range of ground-level ozone concentrations at a range of nitrogen loads. Journal of Plant Physiology 211, 42–52.
| Leaf traits and photosynthetic responses of Betula pendula saplings to a range of ground-level ozone concentrations at a range of nitrogen loads.Crossref | GoogleScholarGoogle Scholar | 28152417PubMed |
Hasanuzzaman M, Borhannuddin Bhuyan MHM, Anee TI, Parvin K, Nahar K, Mahmud JAI, Fujita M (2019) Regulation of ascorbate–glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8, 384
| Regulation of ascorbate–glutathione pathway in mitigating oxidative damage in plants under abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
IPCC (Intergovernmental Panel on Climate Change) (2013) Climatic change 2013: the physical science basis. In ‘IPCC Fifth Assessment Report: underlying scientific–technical assessment.’ Working Group I contribution. Final Draft. Available at http://www.ipcc.ch. [Verified 20 October 2020].
Keller T, Schwager H (1977) Air pollution and ascorbic acid. European Journal of Forest Pathology 7, 338–350.
| Air pollution and ascorbic acid.Crossref | GoogleScholarGoogle Scholar |
Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of a chlorophyll mutant of barley. Canadian Journal of Botany 41, 1053–1062.
| Plastid structure, chlorophyll concentration and free amino acid composition of a chlorophyll mutant of barley.Crossref | GoogleScholarGoogle Scholar |
Maurer S, Matyssek R (1997) Nutrition and the ozone sensitivity of birch (Betula pendula). Trees 12, 1–10.
| Nutrition and the ozone sensitivity of birch (Betula pendula).Crossref | GoogleScholarGoogle 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. Annual Review of Energy and the Environment 26, 237–268.
| Protecting agricultural crops from the effects of tropospheric ozone exposure: reconciling science and standard setting in United States, Europe and Asia.Crossref | GoogleScholarGoogle Scholar |
Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Van Breusegem F, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signaling. Journal of Experimental Botany 67, 3831–3844.
| Spreading the news: subcellular and organellar reactive oxygen species production and signaling.Crossref | GoogleScholarGoogle Scholar | 26976816PubMed |
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
| Reactive oxygen species homeostasis and signaling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia B (2012) Glutathione in plants: an integrated overview. Plant, Cell & Environment 35, 454–484.
| Glutathione in plants: an integrated overview.Crossref | GoogleScholarGoogle Scholar |
Oksanen E, Pandey V, Pandey AK, Keski-Saari S, Kontunen-Soppela S, Sharma C (2013) Impacts of increasing ozone on Indian plants. Environmental Pollution 177, 189–200.
| Impacts of increasing ozone on Indian plants.Crossref | GoogleScholarGoogle Scholar | 23466168PubMed |
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 ethylene-diurea studies. The Science of the Total Environment 532, 230–238.
| Searching for common responsive parameters for ozone tolerance in 18 rice cultivars in India: results from ethylene-diurea studies.Crossref | GoogleScholarGoogle Scholar | 26071964PubMed |
Pellegrini E, Trivellini A, Cotrozzi L, Vernieri P, Nali C (2016). Involvement of phytohormones in plant responses to ozone. In ‘Plant hormones under challenging environmental factors’. (Eds JA Golam and Y Jingquan.) pp. 215–245. (Springer: The Netherlands)
Pellegrini E, Campanella A, Cotrozzi L, Tonelli M, Nali C, Lorenzini G (2018) What about the detoxification mechanisms underlying ozone sensitivity in Liriodendron tulipifera? Environmental Science and Pollution Research International 25, 8148–8160.
| What about the detoxification mechanisms underlying ozone sensitivity in Liriodendron tulipifera?Crossref | GoogleScholarGoogle Scholar | 28357799PubMed |
Pleijel H, Broberg MC, Uddling J, Mills G (2018) Current surface ozone concentrations significantly decrease wheat growth, yield and quality. The Science of the Total Environment 613–614, 687–692.
| Current surface ozone concentrations significantly decrease wheat growth, yield and quality.Crossref | GoogleScholarGoogle Scholar | 28938211PubMed |
Podda A, Pisuttu C, Hoshika Y, Pellegrini E, Carrari E, Lorenzini G, Nali C, Cotrozzi L, Zhang L, Baraldi R, Neri L, Paoletti E (2019) Can nutrient fertilization mitigate the effects of ozone exposure on an ozone-sensitive poplar clone? The Science of the Total Environment 657, 340–350.
| Can nutrient fertilization mitigate the effects of ozone exposure on an ozone-sensitive poplar clone?Crossref | GoogleScholarGoogle Scholar | 30550899PubMed |
Polle A (1996) Mehler reaction: friend or foe in photosynthesis. Botanica Acta 109, 84–89.
| Mehler reaction: friend or foe in photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Rao MV, Koch JR, Davis KR (2000) Ozone: a tool for probing programmed cell death in plants. Plant Molecular Biology 44, 345–358.
| Ozone: a tool for probing programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 11199393PubMed |
Revell LE, Tummon F, Stenke A, Sukhodolov T, Coulon A, Rozanov E, Garny H, Grewe V, Peter T (2015) Drivers of the tropospheric ozone budget throughout the 21st century under the medium-high climate scenario RCP 6.0. Atmospheric Chemistry and Physics 15, 5887–5902.
| Drivers of the tropospheric ozone budget throughout the 21st century under the medium-high climate scenario RCP 6.0.Crossref | GoogleScholarGoogle Scholar |
Tai AP, Martin MV, Heald CL (2014) Threat to future global food security from climate change and ozone air pollution. Nature Climate Change 4, 817–821.
| Threat to future global food security from climate change and ozone air pollution.Crossref | GoogleScholarGoogle Scholar |
Tiwari S, Agrawal M (2018). ‘Tropospheric ozone and its impacts on crop plants: a threat to future global food security.’ (Springer: Switzerland)
Ueda Y, Uehara N, Sasaki H, Kobayashi K, Yamakawa T (2013) Impacts of acute ozone stress on superoxide dismutase (SOD) expression and reactive oxygen species (ROS) formation in rice leaves. Plant Physiology and Biochemistry 70, 396–402.
| Impacts of acute ozone stress on superoxide dismutase (SOD) expression and reactive oxygen species (ROS) formation in rice leaves.Crossref | GoogleScholarGoogle Scholar | 23831949PubMed |
Vainonen JP, Kangasjarvi J (2015) Plant signalling in acute ozone exposure. Plant, Cell & Environment 38, 240–252.
| Plant signalling in acute ozone exposure.Crossref | GoogleScholarGoogle Scholar |
Wang J, Zeng Q, Zhu J, Chen C, Liu G, Teng H (2014) Apoplastic antioxidant enzyme responses to chronic free-air ozone exposure in two different ozone-sensitive wheat cultivars. Plant Physiology and Biochemistry 82, 183–193.
| Apoplastic antioxidant enzyme responses to chronic free-air ozone exposure in two different ozone-sensitive wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 24973575PubMed |
Watanabe M, Yamaguchi M, Matsumura H, Kohno Y, Izuta T (2012) Risk assessment of ozone impact on Fagus crenata in Japan: consideration of atmospheric nitrogen deposition. European Journal of Medical Research 131, 475–484.
Wilkinson S, Mills G, Illidge R, Davies WJ (2012) How is ozone pollution reducing our food supply? Journal of Experimental Botany 63, 527–536.
| How is ozone pollution reducing our food supply?Crossref | GoogleScholarGoogle Scholar | 22016429PubMed |
Yadav DS, Rai R, Mishra AK, Chaudhary N, Mukherjee A, Agrawal SB, Agrawal M (2019) ROS production and its detoxification in early and late sown cultivars of wheat under future O3 concentration. The Science of the Total Environment 659, 200–210.
| ROS production and its detoxification in early and late sown cultivars of wheat under future O3 concentration.Crossref | GoogleScholarGoogle Scholar | 30599339PubMed |
Yamaguchi M, Watanabe M, Iwasaki M, Tabe C, Matsumura H, Kohno Y, Izuta T (2007a) Growth and photosynthetic responses of Fagus crenata seedlings to O3 under different nitrogen loads. Trees 21, 707–718.
| Growth and photosynthetic responses of Fagus crenata seedlings to O3 under different nitrogen loads.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi M, Watanabe M, Matsuo N, Naba J, Funada R, Fukami M, Matsumura H, Kohno Y, Izuta T (2007b) Effects of nitrogen supply on the sensitivity to O3 of growth and photosynthesis of Japanese beech (Fagus crenata) seedlings. Water, Air, and Soil Pollution 7, 131–136.
| Effects of nitrogen supply on the sensitivity to O3 of growth and photosynthesis of Japanese beech (Fagus crenata) seedlings.Crossref | GoogleScholarGoogle Scholar |
Zhang L, Hoshika Y, Carrari E, Paoletti E (2018a) Ozone risk assessment is affected by nutrient availability: evidence from a simulation experiment under free air-controlled exposure (FACE). Environmental Pollution 238, 812–822.
| Ozone risk assessment is affected by nutrient availability: evidence from a simulation experiment under free air-controlled exposure (FACE).Crossref | GoogleScholarGoogle Scholar | 29627751PubMed |
Zhang L, Hoshika Y, Carrari E, Cotrozzi L, Pellegrini E, Paoletti E (2018b) Effects of nitrogen and phosphorus imbalance on photosynthetic traits of poplar Oxford clone under ozone pollution. Journal of Plant Research 131, 915–924.
| Effects of nitrogen and phosphorus imbalance on photosynthetic traits of poplar Oxford clone under ozone pollution.Crossref | GoogleScholarGoogle Scholar | 30426334PubMed |
