Air pollution affects food security in China: taking ozone as an example

Air pollution is becoming an increasingly important environmental concern due to its visible negative impact on human health. However, air pollution also affects agricultural crops or food security directly or indirectly, which has not so far received suf ﬁ cient attention. In this overview, we take ozone (O 3 ) as an example to analyze the principles and extent of the impact of air pollution on food security in China based on a review of the literature. Current O 3 pollution shows a clear negative impact on food security, causing around a 10 % yield decrease for major cereal crops according to a large number of ﬁ eld studies around the world. The mean yield decrease of winter wheat is predicted to be up to 20 % in China, based on the projection of future ground-level O 3 concentration in 2020, if no pollution control measures are implemented. Strict mitigation of NO x and VOC s (two major precursors of O 3 ) emissions is crucial for reducing the negative impacts of ground-level O 3 on food security. Breeding new crop cultivars with tolerance to high ground-level O 3 should receive serious consideration in future research programs. In addition, integrated soil-crop system management will be an important option to mitigate the negative effects of elevated ground-level O 3 on cereal crop production and food quality.


Introduction
Air pollution has been a serious environmental concern in China since the 1980s [1,2] . Among various atmospheric pollutants (e.g., fine particulate matter, NO x , SO 2 and VOC s ), ground-level ozone (O 3 ) has been assumed to be the most phytotoxic air pollutant due to significant damage to plants and the rising trend in the concentration at a regional scale [3] . With the rapid industrialization and urbanization over the last two decades, O 3 concentration has risen at a much higher rate in China than in other countries and the mean daily (24 h average) O 3 concentration reaches more than 50 ppb during the crop growing season in some regions of China [4,5] . Ground-level O 3 concentration in China coincided with the emission of NO x because the latter is one of the most important precursors of O 3 [6][7][8] . Published results show that ambient O 3 concentrations with an average of 40 ppb have significantly decreased the yield of major food crops (including potato, rice, soybean and wheat) by about 10% compared with O 3free air [9] . A field survey around Beijing found a total of 28 species or cultivars exhibiting typical symptoms of O 3 damage [10] . Therefore, it can be inferred that food security in China is being or has already been affected by current O 3 concentrations and this damage will continue in the future. In this manuscript, we review the current and future O 3 pollution, and its impacts on the production of food crop throughout China. In contrast, tropospheric O 3 is known as bad O 3 due to its greenhouse effect and toxicity. In the troposphere, O 3 absorbs infrared rays emanating from the Earth and its radiative power ranks third in the atmosphere after carbon dioxide and methane [11] . The greenhouse effect of this O 3 is more significant in the upper troposphere than in other layers. However, O 3 at ground level mainly acts as a major air pollutant and is one of the main oxidants. It is also known to cause photochemical smog, which disturbs human respiratory functions and plant photosynthesis. Ground-level O 3 is produced from the photochemical reaction of nitrogen oxides (NO x ) and volatile organic compounds (VOC s ) under sunlight (Fig. 1). The amount of O 3 generated by photochemical reaction of air pollutants is much larger than the inflow from the stratosphere. Therefore, O 3 concentrations are strongly affected by human activities.
Tropospheric O 3 has been a global air pollution problem. Currently, the O 3 concentration on a global scale has reached about 40 ppb due to a high use of fossil fuels and it has risen at a rate of 0.5%-2.0% per year since the preindustrial era [11] . O 3 pollution is highest in Central Europe, Eastern China, and the Eastern USA in the world. In Europe, the highest O 3 levels occur in Central and Southern Europe [3] . Nearly one quarter of the earth's surface is currently at risk from elevated O 3 concentrations in excess of 60 ppb during midsummer, with even greater concentrations occurring locally [12] . Models have pre-dicted that tropospheric O 3 concentration could rise by 20%-25% between 2015 and 2050, and further increase by 40%-60% by 2100, if current emission trends continue [13] .
In most parts of China, ground-level O 3 has been the main air pollutant in summer due to the high emission of NO x from a rapid increase in the number and use of automobiles. The highest hourly O 3 concentration was observed to be 316 ppb in the North China Plain [14] . In recent years, the summertime O 3 concentration frequently exceeded the second national standard level (i.e., hourly O 3 concentration: 200 µg$m -3 or approximately 100 ppb) for human health issued by the Chinese Environmental Protection Agency. Due to unbalanced development in the economy and in urbanization between regions, O 3 concentrations differ among geographical locations. In the central and northern part of China, the O 3 reaches a maximum in summer. However, in southern China, the O 3 concentration is generally characterized by a peak in fall and a trough in summer [6,7] . On the monthly-mean basis, ground-level O 3 peaks in May in the Yangtze River Delta, June in the North China Plain, and October in the Pearl River Delta [15] . The annual mean background O 3 concentration over China shows a spatial gradient from 33.7 ppb in the South China to 23.5 ppb in the North and North-east China [6,7] .
Due to significant NO x titration effect in cities, O 3 concentration is lower in cities than rural regions. Fig. 2 shows the diurnal O 3 concentration monitored in the city  [3] . Besides O 3 deposition directly from stratosphere to troposphere, secondarily O 3 in the troposphere formed from reactions of NO x (sum of NO and NO 2 ) and VOC s (e.g., NMHC s , CH 4 , CO) under sunlight is the major contributor to surface O 3 on earth. and cropland in rural regions. The peak of O 3 concentration in rural regions appears earlier and it lasts longer from 3 to 4 p.m. to 8 p.m. in urban regions compared with rural regions. This O 3 concentration difference is quite common. Furthermore, the emission of NO x in China will continue increasing for some decades due to the rapid rise in the use of automobiles and industrial activity [6,7] , so the concentrations of ground-level O 3 are predicted to increase in the future. Therefore, it can be inferred that the high groundlevel O 3 concentration in China, particularly in rural regions, negatively affect food security given that the measured concentrations exceed the critical level of O 3 for crop production [16] . The phytotoxicity of O 3 to plants derives primarily from its oxidative damage to the plasma membranes [17] . Heath et al. [18] reviewed the interaction of O 3 and plant tissues, and proposed three distinct processes: external O 3 concentration, uptake, and detoxification. It is well known that O 3 penetrates plant leaves through open stomata and dissolves into the apoplastic fluid, suggesting that plants with large stomatal conductance would allow a higher O 3 uptake, and thus experience more damage [19][20][21] . Following its entry into leaves through open stomata, O 3 is dissolved in the liquid phase of the apoplastic space surrounding the substomatal cavity [22,23] , and produces a series of reactive oxygen species including hydroxyl radical, singlet oxygen and hydrogen peroxide, which could cause severe damage to cellular components such as membranes and chloroplasts [24][25][26] . High O 3 concentration also reduces the central biochemical processes controlling photosynthesis, such as the maximum carboxylation efficiency, and the maximum rate of ribulose bisphosphate regeneration [27,28] , thus decreasing the light and dark reactions of photosynthesis, causing a range of adverse effects on plants including reduced photosynthetic activity, altered carbon allocation, diminished biomass accumulation, reduced yield and accelerated senescence, with or without visible injury [28][29][30] . Ground-level O 3 pollution negatively affects grain yield and quality of food crops mainly due to its oxidative damage during the growth period in particular the grain filling stage.

Effect of O 3 pollution on cereal crop production and food quality
Experiments in Europe, Japan and the United States indicate that yield losses of agricultural crops may occur even under current O 3 concentrations. Surrounding Beijing, 28 plant species/cultivars including amenity trees, natural forest species and crops (e.g., peanut and snap bean) were found with typical O 3 symptoms during a recent O 3 injury survey [10] . On the basis of open-top chamber results, a meta-analysis showed that the yield of cereal crops including rice, soybean and wheat was reduced by about 8% when ambient O 3 concentration reach 40 ppb [9] . This suggests that food production in China will be partly reduced by the current O 3 concentrations. There have been some field studies to investigate the impact of elevated O 3 on the food crops (winter wheat, rice and oilseed rape) and details can be found in a review by Feng et al. [6] .
In an open top chamber experiment lasting 5 years, wheat yields decreased by 8.5%-58.0% and 40%-73% and rice yields by 10%-34% and 16%-43% as compared with charcoal filtered air for O 3 -1 (75 or 100 ppb) and O 3 -2 (150 or 200 ppb) treatments [31] , respectively. While at the Jiangdu site, a mean of 25% enhancement above the ambient O 3 concentration (A-O 3 , 45.7 ppb) reduced grain yield in winter wheat by 20% with significant variation in the range from 10% to 35% among the various combinations of cultivar and season [30] . In rice, elevated O 3 also reduced the grain yield by 12% on average across four cultivars. However, there were large differences in the extent of these yield losses [32] . These reduced yields caused by O 3 pollution were similar to a recent report by Rai and Agrawal [33] , who summarized the impact of tropospheric O 3 on crop plants worldwide. However, the quantitative assessment of ambient O 3 effects on food crop yield is rare in China. It is necessary to launch large joint programs to assess the current O 3 effects on food crop production and develop a critical O 3 standard to protect crops against O 3 .
Due to the limited number of O 3 impact studies in China and large regional differences in climate, cultivars and management, there are many uncertainties to assess when studying the O 3 effects on food crops in China. So far, there have been only three studies estimating the yield loss of food crops at current and projected O 3 concentrations on a national scale, and there were large differences in O 3 dose responses, even within each study [6,7] . Of these, only the study by Tang et al. [4] is based on the one doseresponse relationship from the field experiment of four local cultivars in subtropical regions of China. Their results indicated that the ground-level O 3 concentration in 2000 caused an estimated yield loss in wheat of 6.4%-15.0% throughout China. Projected to 2020, the O 3 is estimated to induce yield loss of winter wheat in China of 15%-23% [4] , which is much higher than the results from Aunan et al. [34] and Wang and Mauzerall [35] .
On the basis of research conducted in open-top chambers and O 3 -free air concentration enrichment, a recent meta-analysis on grain quality of wheat in response to O 3 showed that O 3 significantly decreased starch concentration. O 3 increased grain protein content and the concentration of several nutritionally important minerals (P, K, Ca, Mg, Cu, Zn, and Mn), but reduced yield [29,36] . Some baking properties (Zeleny value and Hagberg falling number) were positively influenced by ground-level O 3 [36] . It is projected that NO x , VOC s and O 3 concentrations will continue to rise in China in the future. It can be inferred that crops will be exposed to higher levels of O 3 stress, and economic losses will affect not only China but also the neighboring countries (e.g., Japan, Korea, Europe, USA) through long-range transport of both NO x and O 3 . In Europe and North America, air quality and ground-level O 3 concentration has decreased substantially with strict air pollution control measures implemented since the 1990s [37] . Most of the ground-level O 3 was produced from the photochemical reaction of NO x and VOC s under sunlight. Therefore, the most effective measure to reduce O 3 concentration is to mitigate the emissions of O 3 precursors such as NO x and VOC s , which are mainly from automotive exhaust. Three national actions by policy makers will be implemented in order to achieve the goal of lower ground-level O 3 pollution. The first action is to use the Euro standard V for automotive exhaust, which will be enforced throughout China by 2020. The second is to use electric vehicles widely, which has been encouraged by the central and local governments through different preferential policies, such as refunds and tax exemptions. The third is to reduce the total number of automobiles (especially private cars) on road by further developing public transportation in major and populous cities, increasing parking charges and taxation of cars entering city centers.

Breeding crop cultivars tolerant to ground-level O 3 pollution
Due to the fact that plant species and cultivars vary greatly in tolerance [20,27,38,39] , breeding O 3 -tolerant genotypes is a further good method to reduce yield loss. Some genes conferring O 3 tolerance have been found in rice and soybean [40][41][42] and O 3 tolerance genes could be added to other crops using modern molecular biology techniques. There is a strong need for new crop breeding programs to include breeding crop cultivars tolerant to air pollution. This is especially urgent for O 3 tolerant breeding as ground-level O 3 concentrations are rapidly increasing in developing nations like China and India. 4.3 Integrated soil-crop system management for reducing ground-level O 3 pollution impacts Besides air pollution control measures and adoption of O 3 tolerant crop cultivars, integrated soil-crop system management [43,44] is another important option to improve food security and nutrient resource use efficiency even with air pollution such as elevated O 3 . The integrated soil-crop system management will promote a healthy crop canopy formation and match crop nutrient requirement by supplying nutrients in both space and time (Fig. 3). Therefore the soil-crop system management measures (including optimized plant density, crop residue retention, and real-time N management) will help to build a good buffering system for crops even under O 3 pollution. Although no field studies have systematically evaluated the impact of integrated soil-crop system management on crop yield, we believe at least half of the yield loss can be avoided by such integrated measures. For example, Hewitta et al. [45] observed that N management, as part of soil-crop system management, is essential to prevent tropical oil palm plantations from ground-level O 3 pollution. Future studies of the effects of ground-level O 3 pollution should evaluate the effectiveness of integrated soil-crop system management on the production and grain quality of food crops.

Conclusions
With continuing increases in emissions of O 3 precursors such as NO x and VOCs in China with its rapid economic growth, air pollution, especially ground-level O 3 will increase drastically over the coming decades. There is a lack of systematic studies on air pollution effects on crop production and food security in China. Based on a limited literature search, we have selected O 3 pollution as an example to demonstrate the principles and extents of air pollution impact on food security in China. Current O 3 pollution can cause 6.4%-15.0% yield loss for major cereal crops according to a number of O 3 -free air concentration enrichment studies. The mean yield loss of cereal crops could reach more than 20% according to the ground-level O 3 concentrations projected for 2020. To avoid yield damage by O 3 pollution, three strategies need to be seriously considered for the future. The first strategy is strict mitigation of NO x and VOC s emissions to reduce the ground-level O 3 concentration and its negative impact on food security. The second strategy is to breed and adopt new crop cultivars tolerant to high ground-level O 3 concentrations. The third strategy is to adopt integrated soil-crop system management, which will improve food security via increasing the buffering capacity of the soilcrop ecosystems to various air pollutants including O 3 .