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Physiological, biochemical, and molecular responses of rice (Oryza sativa L.) towards elevated ozone tolerance

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Abstract

Rice (Oryza sativa L.) is one of the most important staple food crops that is cultivated in South East Asia. This crop is affected by a wide range of biotic and abiotic factors, each of which is contributing to a change in its physiology, biochemistry, and genetic makeup. Ozone is produced in the troposphere as a result of reactions between abiotic factors, such as oxides of nitrogen and carbon, and UV radiation. These reactions lead to the production of a wide variety of volatile organic compounds. Rice scientists have expressed a great deal of concern regarding the impact of ozone on rice, which has necessitated the development of strategies to combat the problem. The recent advances in rice genomics have led to the discovery of molecular biology approaches such as marker-assisted selection involving quantitative trait loci linked to genes that confer tolerance to ozone stress. This trait is thought to be controlled by a large number of loci with medium effects rather than by a single locus with a large effect. The current review is an effort to provide information on the physiological, biochemical, and molecular responses of rice towards elevated ozone tolerance and also to reflect the available strategies to minimize the effect.

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References

  • Ainsworth EA (2008) Rice production in a changing climate: a meta-analysis of elevated carbon dioxide and elevated ozone concentration responses. Glob Change Biol 14(7):1642–1650

    Article  Google Scholar 

  • Akhtar N, Yamaguchi M, Inada H, Hoshino D, Kondo T, Fukami M, Izuta T (2010) Effects of Ozone on growth, yield, and leaf gas exchange rates of four Bangladeshi cultivars of rice (Oryza sativa L.). Environ Pollut 158(9):2970–2976

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2016) Plant responses to light stress: oxidative damages, photoprotection, and role of phytohormones. In: Plant hormones under challenging environmental factors, pp 181–213. Springer, Dordrecht

  • Bharati K, Mohanty SR, Rao VR, Adhya TK (2001) Influence of flooded and non-flooded condition on CH4-efflux from two soils planted to rice. Chemosphere Glob Change Sci 3(1):25–32

    Article  CAS  Google Scholar 

  • Booker F, Burkey K, Morgan P, Fiscus E, Jones A (2012) Minimal influence of G-protein null mutations on ozone-induced changes in gene expression, foliar injury, gas exchange and peroxidase activity in Arabidopsis thaliana L. Plant Cell Environ 35(4):668–681

    Article  CAS  PubMed  Google Scholar 

  • Carter CA, Cui X, Ding A, Ghanem D, Jiang F, Yi F, Zhong F (2017) Stage-specific, nonlinear surface ozone damage to rice production in China. Sci Rep 7(1):1–6

    Article  Google Scholar 

  • Chen Z, Wang XK, Yao FF, Zheng FX, Feng ZZ (2010) Elevated ozone changed soil microbial community in a rice paddy. Soil Sci Soc Am J 74(3):829–837

    Article  CAS  Google Scholar 

  • Cho K, Shibato J, Agrawal GK, Jung YH, Kubo A, Jwa NS, Rakwal R (2008) Integrated transcriptomics, proteomics, and metabolomics analyses to survey ozone responses in the leaves of rice seedling. J Proteome Res 7(7):2980–2998

    Article  CAS  PubMed  Google Scholar 

  • Conrad R (2002) Control of microbial methane production in wetland rice fields. Nutr Cycl Agroecosyst 64(1):59–69

    Article  CAS  Google Scholar 

  • Dash M, Sahoo JP, Samal KC (2020) Climate Change: It’s Impact on Biodiversity and Human Society. Biotica Res Today 2(6):484–486

    Google Scholar 

  • Dash SSS, Lenka D, Sahoo JP, Tripathy SK, Samal KC, Lenka D, Panda RK (2022). Biochemical characterization of maize (Zea mays L.) hybrids under excessive soil moisture stress. Cereal Res Commun 1–10

  • Debaje SB (2014) Estimated crop yield losses due to surface ozone exposure and economic damage in India. Environ Sci Pollut Res 21(12):7329–7338

    Article  CAS  Google Scholar 

  • Díaz-Torres JDJ, Ojeda-Castillo V, Hernández-Mena L, Vergara-Sánchez J, Saldarriaga-Noreña HA, Murillo-Tovar MA (2022) Long-term analysis of tropospheric ozone in the urban area of Guadalajara, Mexico: a new insight of an alternative criterion. Atmosphere 13(2):152

    Article  Google Scholar 

  • Emberson LD, Büker P, Ashmore MR, Mills G, Jackson LS, Agrawal M, Wahid A (2009) A comparison of North American and Asian exposure-response data for ozone effects on crop yields. Atmos Environ 43(12):1945–1953

    Article  CAS  Google Scholar 

  • EPA (2022) What is ozone and where is it in the atmosphere? Available at: https://www.epa.gov/ozone-pollution-and-your-patients-health/what-ozone. Accessed on: 25th September 2022

  • Feng Y, Yu Y, Tang H, Zu Q, Zhu J, Lin X (2015) The contrasting responses of soil microorganisms in two rice cultivars to elevated ground-level O3. Environ Pollut 197:195–202

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Xu Y, Kobayashi K, Dai L, Zhang T, Agathokleous E, Yue X (2022) Ozone pollution threatens the production of major staple crops in East Asia. Nature Food 3(1):47–56

    Article  CAS  PubMed  Google Scholar 

  • Fowler D, Amann M, Anderson R, Ashmore M, Cox P, Depledge M, Stevenson D (2008) Ground-level ozone in the 21st century: future trends, impacts and policy implications. The Royal Society

  • Frei M (2015) Breeding of ozone resistant rice: Relevance, approaches and challenges. Environ Pollut 197:144–155

    Article  CAS  PubMed  Google Scholar 

  • Frei M, Tanaka JP, Wissuwa M (2008) Genotypic variation in tolerance to elevated ozone in rice: dissection of distinct genetic factors linked to tolerance mechanisms. J Exp Bot 59(13):3741–3752

    Article  CAS  PubMed  Google Scholar 

  • Frei M, Tanaka JP, Chen CP, Wissuwa M (2010) Mechanisms of O3 tolerance in rice: characterization of two QTLs affecting leaf bronzing by gene expression profiling and biochemical analyses. J Exp Bot 61(5):1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Frei M, Kohno Y, Wissuwa M, Makkar HP, Becker K (2011) Negative effects of tropospheric Ozone on the feed value of rice straw are mitigated by an ozone tolerance QTL. Glob Change Biol 17(7):2319–2329

    Article  Google Scholar 

  • Frei M, Wissuwa M, Pariasca-Tanaka J, Chen CP, Südekum KH, Kohno Y (2012) Leaf ascorbic acid level—Is it really important for ozone tolerance in rice? Plant Physiol Biochem 59:63–70

    Article  CAS  PubMed  Google Scholar 

  • Ghude SD, Jena C, Chate DM, Beig G, Pfister GG, Kumar R, Ramanathan V (2014) Reductions in India’s crop yield due to Ozone. Geophys Res Lett 41(15):5685–5691

    Article  Google Scholar 

  • IPCC (1996) Methane Emissions from Rice Cultivation. Available at: https://www.ipcc-nggip.iges.or.jp/public/gl/guidelin/ch4ref5.pdf. Accessed on: 25th September 2022

  • Jing L, Dombinov V, Shen S, Wu Y, Yang L, Wang Y, Frei M (2016) Physiological and genotype-specific factors associated with grain quality changes in rice exposed to high ozone. Environ Pollut 210:397–408

    Article  CAS  PubMed  Google Scholar 

  • Kim KM, Kwon YS, Lee JJ, Eun MY, Sohn JK (2004) QTL mapping and molecular marker analysis for the resistance of rice to ozone. Mol Cells 17(1):151–155

    PubMed  Google Scholar 

  • Kou TJ, Xu GW, Zhu JG (2017) Impact of elevated ozone on nutrient uptake and utilization of Chinese hybrid indica rice (Oryza sativa) cultivars under free-air ozone enrichment. Commun Soil Sci Plant Anal 48(6):635–645

    Article  CAS  Google Scholar 

  • Lakaew K, Akeprathumchai S, Thiravetyan P (2021) Foliar spraying of calcium acetate alleviates yield loss in rice (Oryza sativa L.) by induced anti-oxidative defence system under ozone and heat stresses. Ann Appl Biol 178(2):414–426

    Article  CAS  Google Scholar 

  • Lucht JM (2015) Public acceptance of plant biotechnology and GM crops. Viruses 7(8):4254–4281

    Article  PubMed  PubMed Central  Google Scholar 

  • Macías Benítez S, Navarro Torre S, Caballero Jiménez P, Martín L, Revilla Torres ME, Castaño Navarro A, Parrado Rubio J (2021) Biostimulant capacity of an enzymatic extract from rice bran against ozone-induced damage in Capsicum annum. Front Plant Sci 12:749422

    PubMed  PubMed Central  Google Scholar 

  • McAdam EL, Brodribb TJ, McAdam SA (2017) Does ozone increase ABA levels by non-enzymatic synthesis causing stomata to close. Plant Cell Environ 40(5):741–747

    Article  CAS  PubMed  Google Scholar 

  • Morrell PL, Buckler ES, Ross-Ibarra J (2012) Crop genomics: advances and applications. Nat Rev Genet 13(2):85–96

    Article  CAS  Google Scholar 

  • Oltmans SJ, Lefohn AS, Shadwick D, Harris JM, Scheel HE, Galbally I, Kawasato T (2013) Recent tropospheric ozone changes—a pattern dominated by slow or no growth. Atmos Environ 67:331–351

    Article  CAS  Google Scholar 

  • Peng B, Lai SK, Li PL, Wang YX, Zhu JG, Yang LX, Wang YL (2015) Effects of ozone stress on photosynthesis and dry matter production of rice II-you 084 under different planting densities. Ying Yong Sheng TaiXuebao J Appl Ecol 26(1):17–24

    CAS  Google Scholar 

  • Pramanik K, Sahoo JP, Mohapatra PP, Acharya LK, Jena C (2021) Insights into the embryo rescue-a modern in-vitro crop improvement approach in horticulture. Plant Cell Biotechnol Mol Biol 22(15–16):20–33

    Google Scholar 

  • Quintero-CalderóN EH, SáNchez-Reinoso AD, CháVez-Arias CC, Garces-Varon G, Restrepo-DíAz H (2021) Rice seedlings showed a higher heat tolerance through the foliar application of biostimulants. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 49(1):12120

    Article  Google Scholar 

  • Sahoo JP, Sharma V, Verma RK, Chetia SK, Baruah AR, Modi MK, Yadav VK (2019) Linkage analysis for drought tolerance in kharif rice of Assam using microsatellite markers. Indian J Tradit Knowl 18(2):371–375

    Google Scholar 

  • Sahoo JP, Mohapatra U, Mishra P (2020) An outlook on metabolic pathway engineering in crop plants. Arch Agric Environ Sci 5(3):431–434

    Article  Google Scholar 

  • Sahoo JP, Samal KC, Mishra AP (2021) Provitamin-A biofortified golden rice approved for commercial cultivation in Philippines—a breakthrough in fighting hidden hunger. Biotica Res Today 3(7):648–650

    Google Scholar 

  • Sarkar A, Agrawal SB (2010) Identification of ozone stress in Indian rice through foliar injury and differential protein profile. Environ Monit Assess 161(1):205–215

    Article  CAS  PubMed  Google Scholar 

  • Sarkar A, Singh AA, Agrawal SB, Ahmad A, Rai SP (2015) Cultivar specific variations in antioxidative defense system, genome and proteome of two tropical rice cultivars against ambient and elevated Ozone. Ecotoxicol Environ Saf 115:101–111

    Article  CAS  PubMed  Google Scholar 

  • Sawada H, Komatsu S, Nanjo Y, Khan NA, Kohno Y (2012) Proteomic analysis of rice response involved in reduction of grain yield under elevated ozone stress. Environ Exp Bot 77:108–116

    Article  CAS  Google Scholar 

  • Sawada H, Tsukahara K, Kohno Y, Suzuki K, Nagasawa N, Tamaoki M (2016) Elevated ozone deteriorates grain quality of Japonica Rice cv. Koshihikari, even if it does not cause yield reduction. Rice 9(1):1–10

    Article  Google Scholar 

  • Shah NNAK, Rahman RA, Hashim DM (2015) Changes in physicochemical characteristics of ozone-treated raw white rice. J Food Sci Technol 52(3):1525–1533

    Article  PubMed  Google Scholar 

  • Sharma J, Ravindranath NH (2019) Applying IPCC 2014 framework for hazard-specific vulnerability assessment under climate change. Environ Res Commun 1(5):051004

    Article  Google Scholar 

  • Singh AK, Mitra S, Kar G (2022) Assessing the impact of current tropospheric ozone on yield loss and antioxidant defense of six cultivars of rice using ethylenediurea in the lower Gangetic Plains of India. Environ Sci Pollut Res 1–11

  • Tsukahara K, Sawada H, Matsumura H, Kohno Y, Tamaoki M (2013) Quantitative trait locus analyses of O3-induced grain yield reduction in rice. Environ Exp Bot 88:100–106

    Article  CAS  Google Scholar 

  • Turner NC, Waggoner PE, Rich S (1974) Removal of ozone from the atmosphere by soil and vegetation. Nature 250(5466):486–489

    Article  CAS  Google Scholar 

  • UCAR (2022) Ozone in the Troposphere. Available at: https://scied.ucar.edu/learning-zone/air-quality/ozone-troposphere. Accessed on: 25th September 2022

  • 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 Physiol Biochem 70:396–402

    Article  CAS  PubMed  Google Scholar 

  • Ueda Y, Siddique S, Frei M (2015) A novel gene, Ozone-Responsive Apoplastic Protein 1, enhances cell death in ozone stress in rice. Plant Physiol 169:873–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda Y, Frindte K, Knief C, Ashrafuzzaman MD, Frei M (2016) Effects of elevated tropospheric ozone concentration on the bacterial community in the phyllosphere and rhizoplane of rice. PLoS ONE 11(9):e0163178

    Article  PubMed  PubMed Central  Google Scholar 

  • Vainonen JP, Kangasjärvi J (2015) Plant signalling in acute ozone exposure. Plant Cell Environ 38(2):240–252

    Article  CAS  PubMed  Google Scholar 

  • 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(3):604–618

    Article  Google Scholar 

  • Wahid A, Maggs RSRA, Shamsi SRA, Bell JNB, Ashmore MR (1995) Effects of air pollution on rice yield in the Pakistan Punjab. Environ Pollut 90(3):323–329

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Frei M (2011) Stressed food—the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141(3–4):271–286

    Article  Google Scholar 

  • Wang X, Zhang Q, Zheng F, Zheng Q, Yao F, Chen Z, Lu F (2012) Effects of elevated O3 concentration on winter wheat and rice yields in the Yangtze River Delta, China. Environ Pollut 171:118–125

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Song Q, Frei M, Shao Z, Yang L (2014) Effects of elevated ozone, carbon dioxide, and the combination of both on the grain quality of Chinese hybrid rice. Environ Pollut 189:9–17

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Mills G, Illidge R, Davies WJ (2012) How is ozone pollution reducing our food supply? J Exp Bot 63(2):527–536

    Article  CAS  PubMed  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10(1):1–19

    Article  Google Scholar 

  • Xu M, Yao Q, Chen D, Li M, Li R, Gao B, Chen Z (2021) Estimating the impact of ground ozone concentrations on crop yields across China from 2014 to 2018: a multi-model comparison. Environ Pollut 283:117099

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Hoshino D, Inada H, Akhtar N, Sumioka C, Takeda K, Izuta T (2014) Evaluation of the effects of Ozone on yield of Japanese rice (Oryza sativa L.) based on stomatal ozone uptake. Environ Pollut 184:472–480

    Article  CAS  PubMed  Google Scholar 

  • Yu L, Liu Y, Lu L, Zhang Q, Chen Y, Zhou L, Peng C (2017) Ascorbic acid deficiency leads to increased grain chalkiness in transgenic rice for suppressed of L-GalLDH. J Plant Physiol 211:13–26

    Article  CAS  PubMed  Google Scholar 

  • Zhang WW, Zheng FX, Wang XK, Feng ZZ, Ouyang ZY, Feng ZW (2008) Effects of elevated Ozone on rice (Oryza sativa L.) leaf lipid peroxidation and antioxidant system. Ying Yong Sheng TaiXuebao J Appl Ecol 19(11):2485–2489

    CAS  Google Scholar 

  • Zhang J, Tang H, Zhu J, Lin X, Feng Y (2016) Divergent responses of methanogenic archaeal communities in two rice cultivars to elevated ground-level O3. Environ Pollut 213:127–134

    Article  CAS  PubMed  Google Scholar 

  • Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2(1):1–10

    Article  Google Scholar 

  • Zheng F, Wang X, Zhang W, Hou P, Lu F, Du K, Sun Z (2013) Effects of elevated O3 exposure on nutrient elements and quality of winter wheat and rice grain in Yangtze River Delta, China. Environ Pollut 179:19–26

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Zhou J, Wang Y, Peng B, Zhu J, Yang L, Wang Y (2015) Elevated tropospheric Ozone increased grain protein and amino acid content of a hybrid rice without manipulation by planting density. J Sci Food Agric 95(1):72–78

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Agricultural Biotechnology, Odisha University of Agriculture and Technology, Bhubaneswar, 751003, India

    Jyoti Prakash Sahoo & Kailash Chandra Samal

  2. Department of Plant Breeding and Genetics, Odisha University of Agriculture and Technology, Bhubaneswar, 751003, India

    Pratikshya Mishra

  3. Department of Soil Science and Agricultural Chemistry, Faculty of Agriculture, Sri Sri University, Cuttack, 754006, India

    Ambika Prasad Mishra

  4. Department of Plant Biotechnology, M.S. Swaminathan School of Agriculture, Centurion University of Technology and Management, Paralakhemundi, 761211, India

    Koustava Kumar Panda

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  1. Jyoti Prakash Sahoo
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Contributions

JPS contributed to conceptualization, data curation, formal analysis, investigation, methodology, resources, software, visualization, and writing original draft; PM and APM contributed to editing; KCS and KKP contributed to project administration, supervision, and validation. All authors read and approved the final manuscript.

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Correspondence to Jyoti Prakash Sahoo.

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Communicated by M. Taylor.

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Sahoo, J.P., Mishra, P., Mishra, A.P. et al. Physiological, biochemical, and molecular responses of rice (Oryza sativa L.) towards elevated ozone tolerance. CEREAL RESEARCH COMMUNICATIONS 51, 315–324 (2023). https://doi.org/10.1007/s42976-022-00316-8

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