Abstract
A free air concentration enrichment experiment of different mustard varieties was conducted under elevated (e) ozone (eO3), carbon dioxide (eCO2), a mixture of eO3 × eCO2, and ambient air concentration. The study was conducted to investigate the relationship between plant physiological parameters and changes in atmospheric concentration of O3 and CO2 that may occur under future climates, and to quantify treatment effects on mustard genotypes. Data analysis involved multivariate analysis and the use of linear models that enabled the selection of O3-tolerant and better-performing genotypes under likely future CO2 levels. Plant physiological parameters (namely: total chlorophyll content, leaf area index, antioxidant enzymes and the gas exchange parameters Pn, gs, E, WUE and Tc), and their inter-relationships were measured and recorded at different phenological stages of the crop. All treatments had significant effects on the measured physiological parameters, but differences varied depending upon the physiological stage of the mustard varieties used in the study. The multivariate analysis indicated a strong relationship between measured variables, treatments, and genotypes. Among the three mustard genotypes, ‘Pusa Bold’ (PB) performed better, followed by PM30, particularly under eO3, and PDZM31 was rather sensitive to increased ozone concentration compared with PB and PM30. The results highlighted that all measured physiological parameters were highly sensitive to changes in the relative concentrations of O3, CO2 and their interaction; particularly, the rate of gas exchange between the plant and the atmosphere. Consequently, crop growth and development were affected. The negative effect eO3 was mitigated the presence of eCO2 as shown in the eO3 × eCO2 treatment.
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References
Abebe, A., Pathak, H., Singh, S. D., Bhatia, A., Harit, R. C., & Kumar, V. (2016). Growth, yield, and quality of maize with elevated atmospheric carbon dioxide and temperature in north–west India. Agriculture Ecosystems & Environment,218, 66–72. https://doi.org/10.1016/j.agee.2015.11.014
Aebi, H. (1984). Catalase in vitro. Methods in enzymology, 105, 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Agathokleous, E., Kitao, M., & Koike, T. (2023). Testing phaeophytinization as an index of ozone stress in trees. Journal of Forestry Research,34, 1167–1174. https://doi.org/10.1007/s11676-022-01556-4
Ainsworth, E. A., Lemonnier, P., & Wedow, J. M. (2020). The influence of rising tropospheric carbon dioxide and ozone on plant productivity. Plant Biology,22(S1), 5–11. https://doi.org/10.1111/plb.12973
Ainsworth, E. A., Yendrek, C. R., Sitch, S., Collins, W. J., & Emberson, L. D. (2012). The effects of tropospheric ozone on net primary productivity and implications for climate change. Annual Reviews Plant Biology,63, 637–661. https://doi.org/10.1146/annurev-arplant-042110-103829
Arenque, B. C., Grandis, A., Pocius, O., de Souza, A. P., & Buckeridge, M. S. (2014). Responses of Senna reticulata, a legume tree from the amazonian floodplains, to elevated atmospheric CO2 concentration and waterlogging. Trees,28, 1021–1034. https://doi.org/10.1007/s00468-014-1015-0
Ashrafuzzaman, M., Lubna, F. A., Holtkamp, F., Manning, W. J., Kraska, T., & Frei, M. (2017). Diagnosing ozone stress and differential tolerance in rice (Oryza sativa L.) with ethylenediurea (EDU). Environmental Pollution,230, 339–350. https://doi.org/10.1016/j.envpol.2017.06.055
Bernacchi, C. J., Leakey, A. D., Heady, L. E., Morgan, P. B., Dohleman, F. G., McGrath, J. M., & Ort, D. R. (2006). Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO2 and ozone concentrations for 3 years under fully open-air field conditions. Plant Cell & Environment,29(11), 2077–2090. https://doi.org/10.1111/j.1365-3040.2006.01581.x
Bhatia, A., Kumar, V., Kumar, A., Tomer, R., Singh, B., & Singh, S. (2013). Effect of elevated ozone and carbon dioxide interaction on growth and yield of maize. Maydica,58(3–4), 291–298.
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. Journal of Integrative Plant Biology,51(4), 337–351. https://doi.org/10.1111/j.1744-7909.2008.00805.x
Castillo, F J., Panel, I., & Greppin, H. et al. (1984). Peroxidase release induced by ozone in Sedum album leaves. Plant Physiology. PMC1066779.
Cernusak, L. A., Winter, K., Martínez, C., Correa, E., Aranda, J., Garcia, M., Jaramillo, C., & Turner, B. L. (2011). Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiology,157(1), 372–385. https://doi.org/10.1104/pp.111.182436
Dhaliwal, S. S., Sharma, V., Shukla, A. K., Verma, V., Sandhu, P. S., Behera, S. K., Singh, P., Kaur, J., Singh, H., Abdel-Hafez, S. H., & Gaber, A. (2021). Interactive effects of foliar application of zinc, iron and nitrogen on productivity and nutritional quality of Indian mustard (Brassica juncea L). Agronomy,11(11), 2333. https://doi.org/10.3390/agronomy11112333
Dieleman, W. I. J., Vicca, S., Dijkstra, F., Hagedorn, F., Hovenden, M. J., Larsen, K. S., Morgan, J. A., Volder, A., Beier, C., Dukes, J. S., King, J., Leuzinger, S., Linder, S., Luo, Y., Oren, R., De Angelis, P., Tingey, D., Hoosbeek, M. R., & Janssens, I. (2012). Simple additive effects are rare: A quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Global Change Biology,18(9), 2681–2693. https://doi.org/10.1111/j.1365-2486.2012.02745.x
Fuhrer, J., & Booker, F. (2003). Ecological issues related to ozone: Agricultural issues. Environment International,29(2–3), 141–154. https://doi.org/10.1016/S0160-4120(02)00157-5
Gamar, M. I. A., Kisiala, A., Emery, R. J. N., Yeung, E. C., Stone, S. L., & Qaderi, M. M. (2019). Elevated carbon dioxide decreases the adverse effects of higher temperature and drought stress by mitigating oxidative stress and improving water status in Arabidopsis thaliana. Planta,250, 1191–1214. https://doi.org/10.1007/s00425-019-03213-3
Imai, K., & Ookoshi, T. (2011). Elevated CO2 ameliorates O3-inhibition of growth and yield in paddy rice. Environmental Control in Biology, 49(2), 75–82.
IPCC (2014). Climate change 2014: Synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Available at: https://doi.org/10.1017/CBO9781107415324.
Kaciene, G., Miškelytė, D., AbdElgawad, H., Beemster, G., Asard, H., Dikšaitytė, A., Žaltauskaitė, J., Sujetovienė, G., Januškaitienė, I., & Juknys, R. (2019). O3 pollution in a future climate increases the competition between summer rape and wild mustard. Plant Physiology and Biochemistry,135, 194–205. https://doi.org/10.1016/j.plaphy.2018.11.031
Kimball, B. A., Kobayashi, K., & Bindi, M. (2002). Responses of agricultural crops to free-air CO2 enrichment. Advances in agronomy, 77, 293–368.
Kumar, R., Bhatia, A., Chakrabarti, B., Kumar, V., Tomer, R., Sharma, D. K., & Kumar, S. N. (2021). Effect of elevated ozone and carbon dioxide on growth and yield of rice (Oryza sativa). The Indian Journal of Agricultural Sciences, 91(11).
Kumari, S., Agrawal, M., & Tiwari, S. (2013). Impact of elevated CO2 and elevated O3 on Beta vulgaris L.: Pigments, metabolites, antioxidants, growth, and yield. Environmental Pollution,174, 279–288. https://doi.org/10.1016/j.envpol.2012.11.021
Lamichaney, A., Tewari, K., Basu, P. S., Katiyar, P. K., & Singh, N. P. (2021). Effect of elevated carbon-dioxide on plant growth, physiology, yield and seed quality of chickpea (Cicer arietinum L.) in Indo-Gangetic plains. Physiology and Molecular Biology of Plants, 27, 251–263.
Lamichaney, A., Tewari, K., Katiyar, P. K., Parihar, A. K., Pratap, A., & Singh, F. (2022). Implications of exposing mungbean (Vigna radiata L.) plant to higher CO2 concentration on seed quality. International Journal of Biometeorology,66(12), 2425–2431. https://doi.org/10.1007/s00484-022-02366-3
Lamptey, S., Li, L., Xie, J., Zhang, R., Yeboah, S., & Antille, D. L. (2017). Photosynthetic response of maize to nitrogen fertilization in the semiarid Western Loess Plateau of China. Crop Science,57(5), 2739–2752. https://doi.org/10.2135/cropsci2016.12.1021
Leung, F., Sitch, S., Tai, A. P. K., Wiltshire, A. J., Gornall, J. L., Folbert, G. A., & Unger, N. (2022). CO2 fertilization of crops offsets yield losses due to future surface ozone damage and climate change. Environmental Research Letters,17(7), 074007. https://doi.org/10.1088/1748-9326/ac7246
Manderscheid, R., Erbs, M., & Weigel, H. J. (2014). Interactive effects of free-air CO2 enrichment and drought stress on maize growth. European Journal of Agronomy,52(Part A), 11–21. https://doi.org/10.1016/j.eja.2011.12.007
Maurya, V. K., Gupta, S. K., Sharma, M., Majumder, B., Deeba, F., Pandey, N., & Pandey, V. (2020). Growth, physiological and proteomic responses in field grown wheat varieties exposed to elevated CO2 under high ambient ozone. Physiology and Molecular Biology of Plants,26, 1437–1461. https://doi.org/10.1007/s12298-020-00828-9
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol., 22, 867880.
Pandey, A. K., 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. Agriculture Ecosystems & Environment,196, 158–166. https://doi.org/10.1016/j.agee.2014.07.003
Phothi, R., Umponstira, C., Sarin, C., Siriwong, W., & Nabheerong, N. (2016). Combining effects of ozone and carbon dioxide application on photosynthesis of Thai jasmine rice (Oryza sativa L.) cultivar Khao Dawk Mali 105. Australian Journal of Crop Science,10(4), 591–597. https://doi.org/10.21475/ajcs.2016.10.04.p7595x
Pleijel, H., Broberg, M. C., Uddling, J., & Mills, G. (2018). Current surface ozone concentrations significantly decrease wheat growth, yield and quality. Science of the Total Environment,613, 687–692. https://doi.org/10.1016/j.scitotenv.2017.09.111
Ramakrishnan, S., Dhevagi, P., Poornima, R., Ramya, A., Kannan, B., Chandrakumar, K., Bhaskaran, J., & Boomiraj, K. (2023). Impact of elevated ozone on cabbage. International Journal of Environment and Climate Change,13(11), 176–186. https://doi.org/10.9734/ijecc/2023/v13i113157
Roberts, H. R., Dodd, I. C., Hayes, F., & Ashworth, K. (2022). Chronic tropospheric ozone exposure reduces seed yield and quality in spring and winter oilseed rape. Agricultural and Forest Meteorology, 316, 108859.
Sami, F., Siddiqui, H., Alam, P., & Hayat, S. (2021). Nitric oxide mitigates the salt-induced oxidative damage in mustard by upregulating the activity of various enzymes. Journal of Plant Growth Regulation,40, 2409–2432. https://doi.org/10.1007/s00344-021-10331-4
Singh, R. N., Mukherjee, J., Sehgal, V. K., Bhatia, A., Krishnan, P., Das, D. K., Kumar, V., & Harit, R. (2017). Effect of elevated ozone, carbon dioxide and their interaction on growth, biomass and water use efficiency of chickpea (Cicer arietinum L.). Journal of Agrometeorology,19(4), 301–305. https://doi.org/10.54386/jam.v19i4.595
Singh, S., Bhatia, A., Tomer, R., Kumar, V., Singh, B., & Singh, S. D. (2013). Synergistic action of tropospheric ozone and carbon dioxide on yield and nutritional quality of Indian mustard (Brassica juncea (L.) Czern). Environmental Monitoring and Assessment,185(8), 6517–6529. https://doi.org/10.1007/s10661-012-3043-9
Tai, A. P., Sadiq, M., Pang, J. Y., Yung, D. H., & Feng, Z. (2021). Impacts of surface ozone pollution on global crop yields: Comparing different ozone exposure metrics and incorporating co-effects of CO2. Frontiers in Sustainable Food Systems,5, 534616. https://doi.org/10.3389/fsufs.2021.534616
Tripathi, R., & Agrawal, S. B. (2012). Effects of ambient and elevated level of ozone on Brassica campestris L. with special reference to yield and oil quality parameters. Ecotoxicology and Environmental Safety,85, 1–12. https://doi.org/10.1016/j.ecoenv.2012.08.012
Tripathi, R., Rai, K., Singh, S., Agrawal, M., & Agrawal, S. B. (2019). Role of supplemental UV-B in changing the level of ozone toxicity in two cultivars of sunflower: Growth, seed yield and oil quality. Ecotoxicology,28, 277–293. https://doi.org/10.1007/s10646-019-02020-6
Ulfat, A., Shokat, S., Li, X., Fang, L., Großkinsky, D. K., Majid, S. A., Roitsch, T., & Liu, F. (2021). Elevated carbon dioxide alleviates the negative impact of drought on wheat by modulating plant metabolism and physiology. Agricultural Water Management,250, 106804. https://doi.org/10.1016/j.agwat.2021.106804
Yadav, A., Bhatia, A., Yadav, S., Singh, A., Tomer, R., Harit, R., Kumar, V., & Singh, B. (2021). Growth, yield and quality of maize under ozone and carbon dioxide interaction in North West India. Aerosol and Air Quality Research,21(2), 200194. https://doi.org/10.4209/aaqr.2020.05.0194
Yadava, D. K., Yashpal, Vasudev, S., Singh, N., Saini, N., Prabhu, K. V., Yadav, M. S., Dhillon, M. K., Giri, S. C., Dass, B., & Singh, R. (2019). Indian mustard variety pusa double zero mustard-31 (PDZM-31). Variety notification. Indian Journal of Genetics and Plant Breeding,79(3), 636–637.
Yeboah, S., Zhang, R., Cai, L., Li, L., Xie, J., Luo, Z., Wu, J., & Antille, D. L. (2017). Soil water content and photosynthetic capacity of spring wheat as affected by soil application of nitrogen-enriched biochar in a semiarid environment. Photosynthetica,55(3), 532–542. https://doi.org/10.1007/s11099-016-0672-1
Zheng, G., Chen, J., & Li, W. (2020). Impacts of CO2 elevation on the physiology and seed quality of soybean. Plant Diversity,42(1), 44–51. https://doi.org/10.1016/j.pld.2019.09.004
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The authors are grateful to the Post-Graduate School, ICAR (Indian Agricultural Research Institute), New Delhi, for technical and operational support, and for their help with field and laboratory activities and facilitation of resources required to undertake this research.
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The work reported in this article received financial assistance from the National Innovations on Climate Resilient Agriculture (NICRA) project, ICAR, Government of India.
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GJJ Performed the experiment and drafted the original manuscript. DKS Conceptualization, methodology, Supervision. BK Support to statistical analyses, data curation, draft correction, and formal analyses. AB Provided experimental facility, methodology and formal analysis. SK Instrumental facility, data curation, and draft correction. DLA Editing and formal analysis.
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Jawahar Jothi, G., Sharma, D.K., Kovilpillai, B. et al. Interactive effects of elevated ozone and carbon dioxide on physiological traits of different Indian mustards. Plant Physiol. Rep. 29, 332–342 (2024). https://doi.org/10.1007/s40502-023-00779-9
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DOI: https://doi.org/10.1007/s40502-023-00779-9