Large variability in ambient ozone sensitivity across 19 ethylenediurea-treated Chinese cultivars of soybean is driven by total ascorbate.

The sensitivity of Chinese soybean cultivars to ambient ozone (O3) in the field is unknown, although soybean is a major staple food in China. Using ethylenediurea (EDU) as an O3 protectant, we tested the gas exchange, pigments, antioxidants and biomass of 19 cultivars exposed to 28ppm·hr AOT40 (accumulated O3 over an hourly concentration threshold of 40ppb) over the growing season at a field site in China. By comparing the average biomass with and without EDU, we estimated the cultivar-specific sensitivity to O3 and ranked the cultivars from very tolerant (<10% change) to highly sensitive (>45% change), which helps in choosing the best-suited cultivars for local cultivation. Higher lipid peroxidation and activity of the ascorbate peroxidase enzyme were major responses to O3 damage, which eventually translated into lower biomass production. The constitutional level of total ascorbate in the leaves was the most important parameter explaining O3 sensitivity among these cultivars. Surprisingly, the role of stomatal conductance was insignificant. These results will guide future breeding efforts towards more O3-tolerant cultivars in China, while strategies for implementing control measures of regional O3 pollution are being implemented. Overall, these results suggest that present ambient O3 pollution is a serious concern for soybean in China, which highlights the urgent need for policy-making actions to protect this critical staple food.

[1]  Elena Paoletti,et al.  Ozone levels in European and USA cities are increasing more than at rural sites, while peak values are decreasing. , 2014, Environmental pollution.

[2]  Gang Liu,et al.  A projection of ozone‐induced wheat production loss in China and India for the years 2000 and 2020 with exposure‐based and flux‐based approaches , 2013, Global change biology.

[3]  J. Barnes,et al.  Establishing ozone flux-response relationships for winter wheat: analysis of uncertainties based on data for UK and Polish genotypes. , 2010 .

[4]  Zhilin Zhu,et al.  Ozone concentrations, flux and potential effect on yield during wheat growth in the Northwest-Shandong Plain of China. , 2015, Journal of environmental sciences.

[5]  A. Lefohn,et al.  Responses of human health and vegetation exposure metrics to changes in ozone concentration distributions in the European Union, United States, and China , 2017 .

[6]  M. Agrawal,et al.  Differential protection of ethylenediurea (EDU) against ambient ozone for five cultivars of tropical wheat. , 2009, Environmental pollution.

[7]  H. Harmens,et al.  Ozone and plants. , 2015, Environmental pollution.

[8]  Yu Song,et al.  An economic assessment of the health effects and crop yield losses caused by air pollution in mainland China. , 2017, Journal of environmental sciences.

[9]  S. Krupa,et al.  The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. , 2009, Journal of integrative plant biology.

[10]  E. Paoletti,et al.  Effects of a three-year exposure to ambient ozone on biomass allocation in poplar using ethylenediurea. , 2013, Environmental pollution.

[11]  E. Paoletti,et al.  Both ozone exposure and soil water stress are able to induce stomatal sluggishness , 2013 .

[12]  E. Paoletti,et al.  Effects of long-term ambient ozone exposure on biomass and wood traits in poplar treated with ethylenediurea (EDU). , 2015, Environmental pollution.

[13]  M. Plöchl,et al.  Simulating ozone detoxification in the leaf apoplast through the direct reaction with ascorbate , 2000, Planta.

[14]  H. Velthuizen,et al.  Limited potential of crop management for mitigating surface ozone impacts on global food supply , 2011 .

[15]  H. Aebi,et al.  Catalase in vitro. , 1984, Methods in enzymology.

[16]  M. Sanz,et al.  Ozone Sensitivity Differences in Five Tomato Cultivars: Visible Injury and Effects on Biomass and Fruits , 2007 .

[17]  E. Paoletti,et al.  Ethylenediurea (EDU): a research tool for assessment and verification of the effects of ground level ozone on plants under natural conditions. , 2011, Environmental pollution.

[18]  M. Yamaguchi,et al.  Relationship between cultivar difference in the sensitivity of net photosynthesis to ozone and reactive oxygen species scavenging system in Japanese winter wheat (Triticum aestivum). , 2012, Physiologia plantarum.

[19]  I. Mateos-Aparicio,et al.  Soybean, a promising health source. , 2008, Nutricion hospitalaria.

[20]  K. Burkey,et al.  Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning , 2005 .

[21]  Zhaozhong Feng,et al.  Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis , 2009 .

[22]  A. Wahid,et al.  Effects of ozone on crops in north-west Pakistan. , 2013, Environmental pollution.

[23]  K. Asada,et al.  Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts , 1981 .

[24]  D. K. Biswas,et al.  Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years , 2007 .

[25]  F. Hayes,et al.  Assessing the effects of ambient ozone in China on snap bean genotypes by using ethylenediurea (EDU). , 2015, Environmental pollution.

[26]  Gongxuan Zhang,et al.  Mapping ozone risks for rice in China for years 2000 and 2020 with flux-based and exposure-based doses , 2014 .

[27]  Z. Szantoi,et al.  Protection of plants from ambient ozone by applications of ethylenediurea (EDU): a meta-analytic review. , 2010, Environmental pollution.

[28]  S. Long,et al.  How does elevated ozone impact soybean? A meta‐analysis of photosynthesis, growth and yield , 2003 .

[29]  R. K. Kar,et al.  Possible mechanisms of light-induced chlorophyll degradation in senescing leaves of Hydrilla verticillata , 1987 .

[30]  G. Mills,et al.  Has the sensitivity of soybean cultivars to ozone pollution increased with time? An analysis of published dose–response data , 2016, Global Change Biology.

[31]  R. Howell,et al.  Field Assessment of Air Pollution-induced Soybean Yield Losses 1 , 1979 .

[32]  A. Chidthaisong,et al.  Effects of Elevated Ozone Concentrations on Thai Jasmine Rice Cultivars (Oryza Sativa L.) , 2005 .

[33]  J. Carnahan,et al.  Prevention of Ozone Injury to Plants by a New Protectant Chemical , 1978 .

[34]  E. Paoletti,et al.  Impacts of ethylenediurea (EDU) soil drench and foliar spray in Salix sachalinensis protection against O3-induced injury. , 2016, The Science of the total environment.

[35]  Shalini Singh,et al.  Cultivar-Specific Response of Soybean (Glycine max L.) to Ambient and Elevated Concentrations of Ozone Under Open Top Chambers , 2011 .

[36]  Stephen Sitch,et al.  The effects of tropospheric ozone on net primary productivity and implications for climate change. , 2012, Annual review of plant biology.

[37]  R. Nelson,et al.  Ozone Exposure Response for U.S. Soybean Cultivars: Linear Reductions in Photosynthetic Potential, Biomass, and Yield1[W][OA] , 2012, Plant Physiology.

[38]  G. Noctor Metabolic signalling in defence and stress: the central roles of soluble redox couples. , 2006, Plant, cell & environment.

[39]  E. Paoletti Ozone impacts on forests , 2007 .

[40]  L. Packer,et al.  Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. , 1968, Archives of biochemistry and biophysics.

[41]  M. Agrawal,et al.  Application of ethylene diurea (EDU) in assessing the response of a tropical soybean cultivar to ambient O₃: nitrogen metabolism, antioxidants, reproductive development and yield. , 2015, Ecotoxicology and environmental safety.

[42]  E. Paoletti,et al.  High doses of ethylene diurea (EDU) are not toxic to willow and act as nitrogen fertilizer. , 2016, The Science of the total environment.

[43]  Determinants of stomatal sluggishness in ozone-exposed deciduous tree species. , 2014, The Science of the total environment.

[44]  K. Omasa,et al.  A comparison between stomatal ozone uptake and AOT40 of deciduous trees in Japan , 2011 .

[45]  Zhaozhong Feng,et al.  Effects of elevated O3 exposure on seed yield, N concentration and photosynthesis of nine soybean cultivars (Glycine max (L.) Merr.) in Northeast China. , 2014, Plant science : an international journal of experimental plant biology.

[46]  A. Wahid,et al.  Effects of oxidants on soybean growth and yield in the Pakistan Punjab. , 2001, Environmental pollution.

[47]  X. Fang,et al.  Regional differences of vulnerability of food security in China , 2009 .

[48]  Edward H. Lee,et al.  Ozone tolerance and antioxidant enzyme activity in soybean cultivars , 2004, Photosynthesis Research.

[49]  Nianliang Cheng,et al.  Characteristics of Ground Ozone Concentration over Beijing from 2004 to2015: Trends, Transport, and Effects of Reductions , 2016 .

[50]  B. Gimeno,et al.  A synthesis of AOT40-based response functions and critical levels of ozone for agricultural and horticultural crops , 2007 .

[51]  M. Agrawal,et al.  Assessing the impact of ambient ozone on growth and productivity of two cultivars of wheat in India using three rates of application of ethylenediurea (EDU). , 2005, Environmental pollution.

[52]  E. Paoletti,et al.  Protection of ash (Fraxinus excelsior) trees from ozone injury by ethylenediurea (EDU): roles of biochemical changes and decreased stomatal conductance in enhancement of growth. , 2008, Environmental pollution.

[53]  E. Paoletti,et al.  The first toxicological study of the antiozonant and research tool ethylene diurea (EDU) using a Lemna minor L. bioassay: Hints to its mode of action. , 2016, Environmental pollution.

[54]  T. Carter,et al.  Foliar resistance to ozone injury in the genetic base of U.S. and Canadian soybean and prediction of resistance in descendent cultivars using coefficient of parentage , 2009 .

[55]  R. A. Reinert,et al.  Genetic Control of O3 Sensitivity in a Cross Between Two Cultivars of Snap Bean , 2000 .

[56]  M. Agrawal,et al.  Variability in antioxidant and metabolite levels, growth and yield of two soybean varieties: an assessment of anticipated yield losses under projected elevation of ozone. , 2010 .

[57]  J J Strain,et al.  The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. , 1996, Analytical biochemistry.

[58]  I. Hassan Physiological and biochemical response of potato (Solanum tuberosum L. cv. Kara) to O3 and antioxidant chemicals : possible roles of antioxidant enzymes , 2006 .

[59]  E. Ainsworth,et al.  Measurement of reduced, oxidized and total ascorbate content in plants , 2007, Nature Protocols.

[60]  Z. Szantoi,et al.  Use of ethylenediurea (EDU) to ameliorate ozone effects on purple coneflower (Echinacea purpurea). , 2007, Environmental pollution.

[61]  A. Pandey,et al.  Differences in responses of two mustard cultivars to ethylenediurea (EDU) at high ambient ozone concentrations in India , 2014 .

[62]  Jessica L. Neu,et al.  Rapid increases in tropospheric ozone production and export from China , 2015 .

[63]  A. Pandey,et al.  Searching for common responsive parameters for ozone tolerance in 18 rice cultivars in India: Results from ethylenediurea studies. , 2015, The Science of the total environment.

[64]  M. Zhou,et al.  Photosynthesis and biochemical responses to elevated O3 in Plantago major and Sonchus oleraceus growing in a lowland habitat of northern China. , 2017, Journal of environmental sciences.

[65]  H. Lichtenthaler CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[66]  M. Agrawal,et al.  Investigating the response of tropical maize (Zea mays L.) cultivars against elevated levels of O3 at two developmental stages , 2014, Ecotoxicology.

[67]  E. Paoletti,et al.  Use of the antiozonant ethylenediurea (EDU) in Italy: verification of the effects of ambient ozone on crop plants and trees and investigation of EDU's mode of action. , 2009, Environmental pollution.

[68]  R. Funada,et al.  Effects of ozone on growth, yield and leaf gas exchange rates of four Bangladeshi cultivars of rice (Oryza sativa L.). , 2010, Environmental pollution.

[69]  W. Manning,et al.  Factors affecting the effects of EDU on growth and yield of field-grown bush beans (Phaseolus vulgaris L.), with varying degrees of sensitivity to ozone. , 2005, Environmental pollution.

[70]  L. Horowitz,et al.  Global crop yield reductions due to surface ozone exposure: 2. Year 2030 potential crop production losses and economic damage under two scenarios of O3 pollution , 2011 .

[71]  D. Ort,et al.  Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open‐air field conditions , 2011 .

[72]  D. Ort,et al.  Impacts of rising tropospheric ozone on photosynthesis and metabolite levels on field grown soybean. , 2014, Plant science : an international journal of experimental plant biology.