Introduction

Ground-level ozone (O3) is a secondary, short-lived air pollutant (Parrish et al., 2012; Proietti et al., 2021) formed by the photochemical oxidation of NOx in the presence of precursor gases such as carbon monoxide, methane, and volatile organic compounds (Simpson et al., 2015). Ozone is a strong oxidant molecule and plays a crucial role in tropospheric chemistry by controlling the oxidation processes (Kunchala et al., 2021). The lifetime of tropospheric O3 varies between ~ 5 and 30 days, which depends on season and altitude, for instance, the lifetime of O3 is longer in winter season and upper troposphere and vice versa (Parrish et al., 2012). Similarly, concentrations of O3 are high in tropical and subtropical regions as it is naturally appropriate environment (low humidity, high temperature, and high light intensity) for O3 formation (Eghdami et al., 2022; Ziemke et al., 2019).

Tropospheric O3 is a third leading greenhouse gas in terms of radiative forcing (Mickley et al., 2001), which affects climate change (IPCC, 2013) and is considered the most harmful air pollutant for crops, vegetation (Mills et al., 2018b; Sharps et al., 2021; Yadav et al., 2021a), biodiversity (Agathokleous et al., 2020) and ecological systems (Liu et al., 2021). Despite the implementation of air quality legislative standards to control the precursor’s emissions worldwide (Sicard et al., 2016; Simon et al., 2015), current O3 concentrations are still high and can suppress agricultural/horticultural productivity in many countries around the world (Cailleret et al., 2018; Mills et al., 2018a; Proietti et al., 2021). The O3 pollution level has begun to decline mostly in developed countries in North America and Europe, but it continues to rise in rapidly developing countries like China, India, and Brazil (Kunchala et al., 2021; Mills et al., 2018a; Turnock et al., 2018). A report of China suggested a trend of 0.4 ppb per year increase of O3 over East Asia (Chang et al., 2017). Similarly, a 30% O3 increase was observed from 2013 (47.5 ppb) to 2019 (61.8 ppb) at 243 Chinese monitoring sites (Lu et al., 2019; Yuan et al., 2021).

In India, a study by Lal et al. (2012) assessed the pattern of O3 concentration changes over the northeastern Indo-Gangetic plains (IGP) region and reported the largest escalation of 6–7.2% per decade with 0.4 ± 0.25% per year, which shows the severity of O3 risk over the IGP region compared to global O3 pollution rise. The spatiotemporal variabilities in O3 concentration over different parts of India have been investigated by many researchers and ascribed to seasonal and geographical variations, which are further correlated with meteorology (Girach et al., 2017; Nair et al., 2018; Singh & Agrawal, 2017). The pattern of O3 concentration shows 40–60 ppb (higher) range during the pre-monsoon/summer season and 15–20 ppb (lower) range during the monsoon months over the northern, western, and peninsular regions of India (Kunchala et al., 2021). The high O3 concentration over the IGP region of India is now a major concern as it is posing a threat to agricultural productivity (Mukherjee et al., 2020; Singh & Agrawal, 2017).

The severity of O3 impact on plants is attributed to the amount of uptake and its reaction ability with cellular components to generate reactive oxygen species (ROS) (Sicard et al., 2020; Yadav et al., 2019). The O3 nearby the plant enters leaves through the stomata during gaseous exchange, reaches apoplast quickly and reacts to produce ROS such as superoxide, hydrogen peroxide, hydroxyl radical, and singlet oxygen (Janku et al., 2019). The O3-induced ROS further reacts with plant cell organelles and then initiate’s damage at the molecular, biochemical, and physiological levels and accelerates leaf senescence, resulting in a reduction of crop yield. In defense response, O3 exposed plants start additional production of enzymatic and non-enzymatic antioxidants, which play a decisive role in maintaining cellular redox balance by detoxifying the extra ROS molecules (Severino et al., 2007; Yadav et al., 2019). The typical effect of O3 on sensitive plants induced by long-term exposure is early senescence of leaves as a consequence of reduction in photosynthate accumulation in plants and alteration in partitioning of photoassimilates between defense and yield products (Emberson et al., 2018; Yadav et al., 2020a, b). The sensitive plant species show specific O3 injury symptoms, which can be visualized in the form of chlorotic spotting (stipples), mottling, bronzing (red to brown minute spots) and eventually leading to foliar necrotic lesions (interveinal stipple on the adaxial side) (Feng et al., 2014; Hayes et al., 2007; Ladd et al., 2011; Sicard et al., 2021). A typical pattern of O3 injury symptoms is mostly localized on the upper leaf surface (Nali & Lorenzini, 2021). The O3 injury symptoms under ambient conditions are reported in North and South America, Europe, Asia, Australia, and Africa, which suggests that the current situation of O3 concentration is above its phytotoxic threshold across the world (Krupa et al., 2001; Marco et al., 2020).

The damaging effect of O3 on plants has been extensively studied using a series of indices, mainly divided into O3 exposure-based indices such as AOT40 (accumulated ozone over a threshold value of 40 ppb), M12 (12 h mean O3 concentration), M7 (7 h mean O3 concentration), and O3 flux-based indices such as PODYIAM (phytotoxic ozone dose above a threshold flux of Y nmol m−2 s−1, parameterized for integrated assessment modelling), and PODYSPEC (species-specific phytotoxic ozone dose above a threshold flux of Y nmol m−2 s−1) (CLRTAP, 2017; Mills et al., 2018a, b, c; Yadav et al., 2021a). The O3 flux-based indices are relatively complex to obtain, as they consider parameters such as leaf area index, stomatal conductance, weather condition, vapour pressure deficit, soil moisture, phenology, and vegetation characteristics of a plant (Pleijel et al., 2021). Whereas, O3 exposure-based indices are quite straightforward and require only data of O3 measurements nearby the plants (Yadav et al., 2021a). Studies conducted on the basis of flux-effect relationships (POD vs yield) and exposure-yield relationships (AOT40 vs yield) suggested that the stomatal O3 flux-based indices provide a more accurate assessment of O3 risk compared to exposure-based indices (Anav et al., 2016; Proietti et al., 2021). Usually, O3 sensitive plants exhibit high stomatal O3 uptake in leaves, which results in visible symptoms on leaves. The O3 symptoms are more severe in older leaves than the younger ones due to the higher accumulation of stomatal O3 flux into leaves, leading to premature leaf abscission (Sharps et al., 2021). Visible foliar damage to O3 may have economic consequences for crop production and quality (Zhao et al., 2011, 2018).

Keeping these facts in mind, the main focus of this review is to provide complete information on crop’s sensitivity to O3 at the most fertile and O3 polluted IGP region of India based on recent observational methods and studies. For securing the productivity of crops in such a scenario, an interactive mechanism of O3 and nitrogen on plant performance and several future prospects are also discussed.

Indices for evaluating sensitivity of crops to O3

Stomatal O3 uptake (phytotoxic O3 dose: POD)

Recent researches on crop response function against O3 are shifting from exposure (based on O3 concentration: AOT40) to stomatal flux (based on phytotoxic O3 uptake) approach, since it provides physiologically more robust information of O3 risk assessment (Paoletti et al., 2019; Pleijel et al., 2021). At present, phytotoxic ozone dose (POD) represents a strong improvement over AOT40 index. The strength of POD approach is highlighted in the development and application of models used for O3 risk assessment of crops in different regions of the world (Feng et al., 2018; Harmens et al., 2018; Wu et al., 2016; Yadav et al., 2021a). The O3 risk assessment and variability in different crop’s sensitivity are well described in the Convention on Long-Range Transboundary Air Pollution (CLRTAP, 2017). Sensitivity to O3 varied with crop species due to the differences in uptake potential of O3 (Sharps et al., 2021). In addition, stomatal conductance of leaves is greatly influenced by environmental variables such as photosynthetically active radiation, temperature, and air humidity which create dissimilarities in stomatal O3 uptake among crops, species, cultivars, and even plants of the same variety due to the variability in accumulation of POD (Hayes et al., 2019a; Paoletti et al., 2019; Yadav et al., 2021a). Pleijel et al. (2021) have observed that the variations in O3 sensitivity were slightly larger in inter-cultivar than the intra-cultivar with the same input data of POD6 for European wheat. And so also, some important genetic changes among the crop cultivars associated with genotypic differences are responsible for the variations in O3 sensitivity in wheat (Feng et al., 2016) and rice (Ashrafuzzaman et al., 2017; Frei et al., 2012).

Recently, Yadav et al. (2021a) have observed O3 flux-response based modeled approach to identify the critical levels and species-specific O3 sensitivity of four wheat cultivars under Indian climatic conditions using DO3SE model (Deposition of Ozone for Stomatal Exchange: a stomatal flux based model used for assessing O3 risk in crops and tree species) (Table 1). Their study documents that the critical point of accumulation of POD6 was 0.284 mmol O3 m−2 for early sown cultivars and 0.393 mmol O3 m−2 for late sown cultivars, which are responsible for 5% yield losses. This suggests that early sown cultivars are more sensitive to O3 as the critical condition comes at lower accumulation of POD6 than late sown cultivars. Besides, a significant negative linear flux-effect relationship is also assisted in identifying the sensitivity level of wheat cultivars in future O3 situations by the slope coefficient comparison and allows quantitative rating of the sensitivity (Harmens et al., 2018; Pleijel et al., 2014; Wu et al., 2016; Yadav et al., 2021a).

Table 1 Sensitivity of agricultural crops to tropospheric O3 in IGP region
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Visible foliar injury

The O3-injury assessment is an easy, convincing, and reliable method to determine the sensitiveness of a species because the severity of pollutants may differ with different (sensitive/resistant) genotypes (Nali & Lorenzini, 2021). It is also helpful to detect areas of high potential risk (Feng et al., 2014; Sicard et al., 2021). Visible symptoms of O3 are very easy to understand by representatives of the media, policymakers, and non-scientists. After exposure to ambient air containing phytotoxic O3, plants start to change their metabolism, which eventually leads to the formation of visible injury (Krupa et al., 2001). Booker et al. (2009) reported that the visible foliar O3 symptoms in a sensitive (18%) grape variety were more than in a resistant variety (6%) under ambient O3 condition. The visible injury appears after the O3 uptake through stomata reaches a threshold (CLRTAP, 2017). Fernandes and Moura (2021) assessed visible O3 injury development related to PODy in Astronium graveolens Jacq. and confirmed the symptoms by using structural markers attributed to oxidative burst and hypersensitive responses. European programs such as EU/ECE International Co-operative Program (ICP-Forests and ICP-Vegetation) and North American programs such as Forest Health Monitoring Program have incorporated the visible injury assessment records of forest plants, crops, and semi-natural vegetation across Europe and the USA to easily identify the O3 sensitive species in natural field conditions (Feng et al., 2014; Hayes et al., 2007). Some other past reviews have ranked plant species sensitivity to O3 according to O3-induced visible injury (Gerosa et al., 2003; Hoshika et al., 2018; Vanderheyden et al., 2001).

Despite O3 being an important air pollutant in India, visible injury assessment is not attempted throughout the country. Under the exposure of ambient + 30 ppb O3, Singh et al. (2018b) observed interveinal chlorotic and necrotic foliar spots in tested 14 Indian wheat cultivars and categorized them into sensitive, moderately sensitive, and tolerant cultivars on the basis of severity of foliar injury. A study on two mung bean (Vigna radiata L.) cultivars, HUM-2 and HUM-6, exposed to elevated O3 also depicted the foliar injury in the form of interveinal chlorosis on adaxial portion of leaves. High foliar injury in HUM-2 as compared to HUM-6 was found to be related with greater production of ROS and little investment of antioxidant defense machinery (Mishra & Agrawal, 2015). Further, the percentage of injury symptoms on leaves was found to be matched with the yield losses in different cultivars. Chaudhary and Agrawal (2013) also observed foliar O3 injury in 6 clover (Trifolium alexandrinum L.) cultivars under elevated O3 conditions and found that the magnitude of O3 injury symptoms directly corresponded with sensitivity of different cultivars. Wardan and Bundel were found the most sensitive cultivars to O3, showing severe visible O3 injury symptoms. The JHB-146 cultivar was intermediately sensitive with moderate injury symptoms, while Fahli, Saidi, and Mescavi cultivars were ranked under slightly O3 sensitive category due to least injury symptoms.

Cumulative stress response index

Variations in O3 sensitivity among the genotypes of wheat depend on changes in antioxidant defense capacity (Feng et al., 2016). Stress-response related parameters such as accessory pigments, ROS-scavenging metabolites/enzymes production rate (antioxidant), photosynthetic rate, and photoassimilates were measured individually and the percentage changes in each parameter were aggregated and the values were arranged in an order for the ranking of cultivar’s sensitivity to O3 (Singh et al., 2018b). Cumulative stress response index (CSRI) can be used as an important tool to assess the sensitivity of O3 based on antioxidant defense response of plants (Fatima et al., 2019). Singh et al. (2018b) calculated CSRI for 14 Indian wheat cultivars and categorized them into sensitive, intermediately sensitive, and tolerant cultivars (Table 1). Yadav et al. (2019) demonstrated that the O3 sensitivity of wheat cultivars was also attributed to detoxification of O3-induced ROS levels by enzymatic and non-enzymatic antioxidants. The possible energy allocation trade-off between antioxidative defense and photosynthate’s accumulation under elevated O3 levels was cultivar-specific response that influenced cultivar’s productivity (Table 1). Fatima et al. (2018) also suggested that defense mechanism of each wheat cultivar against O3 was different and thus the sensitivity varied. Their study observed that high O3-induced oxidative stress up regulated the enzymatic antioxidants and phenylpropanoid pathway in modern wheat cultivar (HD2987: O3 sensitive cultivar). However, in PBW502 (intermediately O3 sensitive cultivar), enzymatic and non-enzymatic antioxidants were enhanced, while in old cultivar (Kharchiya65: O3 tolerant cultivar), only induction of non-enzymatic antioxidants occurred to combat O3 stress.

Variations in crop species sensitivity to O3

According to the existing information on crop sensitivity to O3, differences in O3 sensitivity are considerably larger for global data sets that reflect local and regional variations in O3 sensitivity. In other words, sensitivity to O3 of same crop species may change across different continents, including tropical, subtropical, and temperate crop-growing regions. However, the sensitivity of crops to O3 is not much explored in every region of the world, only few countries are working such as Europe, China, the USA, India, and Japan. Some recent reports (Hayes et al., 2019b; Sharps et al., 2021) also provide information on African tropical crop responses to O3, particularly wheat (Triticum aestivum L.), sorghum (Sorghum bicolor L.), finger millet (Eleusine coracana L.), pearl millet (Pennisetum glaucum L.), and common bean (Phaseolus vulgaris L.). All these crops have shown visible O3 effect on leaves. The accelerated leaf senescence in African wheat cultivars was a main symptom of high O3 exposure (Sharps et al., 2021).

Wheat cultivar’s sensitivity to O3 has increased progressively over time due to selective breeding plans for enhancing stomatal conductance and yield (Biswas et al., 2008; Pleijel et al., 2006; Yadav et al., 2020a). Moreover, variations in O3 sensitivity of cultivars of a single species used in different continents might be due to the changed selection criteria in different locations, possibly because of suitability in a particular climate. Asian (India, China) wheat and rice cultivars are more sensitive than cultivars of the USA and Europe (Emberson et al., 2009). However, almost nothing is known about the sensitivity of staple African crops to O3 (Harmens et al., 2019). Thus, it is suggested that critical levels of O3 for tropical crops are needed using stomatal O3 flux to take environmental conditions into account to fully quantify the risk to food production (Sharps et al., 2021). Likewise, sensitivity to O3 may differ among distinct crop species. For instance, the average annual global yield losses due to stomatal O3 uptake during 2010–2012 were 4.4, 6.1 and 7.1% for rice, maize and wheat, respectively (Mills et al., 2018c). In recent decades, many studies on agricultural crops over the IGP region have shown the differential sensitivity among cultivars and species and also identified the main causes of O3 sensitivity which are compiled in Table 1.

Losses in productivity due to tropospheric O3

The prevalent occurrence of high O3 concentration is accelerating the loss of crop and vegetable productivity in the predominating fertile agricultural regions of India (Mukherjee et al., 2020; Oksanen et al., 2013). Investigations of crop yield losses due to prevailing high O3 concentration in the IGP region have been attempted by many researchers with different approaches such as exposure-based experiments (Fatima et al., 2019; Ghosh et al., 2020; Yadav et al., 2020a), observation based studies (Kumari et al., 2020; Sinha et al., 2015) and O3 flux-based and model-based approaches (Fischer, 2019; Sharma et al., 2019; Yadav et al., 2021a) which are given in Table 2.

Table 2 Variations in yield losses of crops and vegetables in India
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Exposure-based study

A study in the Delhi NCR region found reductions in rice yield by 6.3% using AOT40 index and 23% by total AOTX (AOT40, AOT30, AOT25, AOT20, AOT15, AOT10, AOT5, and AOT0), while only 2% at M7 index (Saxena et al., 2020). The study also indicated that among all the indices, AOT 40 is the most suitable index for evaluating the impact of O3 on rice in Indian climate. Ramya et al. (2021) estimated the responses of fifteen rice cultivars at a mean 50 ppb O3 for 30 days, and found average reductions of 0.62% in test weight of 1000 seed and 23.83% in straw weight compared to control (Table 2). This finding further revealed intra-species variability in responses of rice cultivars to elevated O3 stress. At ambient O3 concentration, rice cultivar NDR 97 exhibited more reduction in grain yield compared to Saurabh 950. However, more decrement in test weight suggested that number of grains was enhanced but weight of grains decreased (Rai et al., 2010). Two rice cultivars, Shivani and Malviya dhan 36 treated at elevated O3 (ambient + 20 ppb), showed yield reductions by 45 and 39%, respectively (Sarkar & Agrawal, 2012). More reduction in yield of Shivani was ascribed to greater utilization of photoassimilates in alleviating the harmful effects of O3 rather than investment in reproduction (Sarkar et al., 2015) (Table 2). Similarly, Surabhi et al. (2020) reported Pusa Basmati-1, a cultivar of rice, to be more susceptible due to greater yield loss than Sarjoo-52 cultivar under ambient O3 exposure.

In India, yield reductions in wheat due to surface O3 ranged from 11 to 20.7% (Mukherjee et al., 2020). Recently, Mina et al. (2021) reported reductions in grain yield by 9.2% and biomass by 11% in wheat cultivar HD 2967 under elevated O3 (ambient + 70 ppb) using FACE (free-air concentration enrichment). Elevated O3 (ambient + 20 ppb) exposure led to decline in grain weight by 27.3% and harvest index by 16.8%, in HD2967 cultivar of wheat compared to ambient O3 using open top chambers (Ghosh et al., 2021) (Table 2).

At identical O3 concentrations, the variability in crop yield losses was reported mainly due to the distinct sensitivity of cultivars to O3 (Rai et al., 2010; Singh et al., 2018b; Yadav et al., 2019). Modern and old wheat cultivars showed distinct variations in yield and quality parameters under elevated O3, where modern high yielding cultivar was found more susceptible to O3 compared to old low yielding cultivar (Yadav et al., 2020a). Furthermore, fourteen Indian wheat cultivars based on grain yield response under elevated O3 depicted that early released cultivars (before year 2000) were less sensitive compared to newly released cultivars (Singh et al., 2018b) (Table 2). Wheat cultivars (Kharchiya 65-O3 tolerant; PBW-intermediately sensitive and HD 2987-O3 sensitive) selected from study of Singh et al. (2018b) were further examined for the impact of elevated O3 on yield attributes. Losses in test weight by 12.9% in Kharchiya 65, 27.1% in PBW and 42.2% in HD 2987 were observed (Fatima et al., 2018). Similarly, Mishra et al. (2013) observed reductions in grain weight plant−1 in both dwarf (HUW-37) and tall (K-9107) cultivars of wheat under elevated O3 (ambient + 10 ppb) (Table 2). However, dwarf cultivar having better yield was found to be more susceptible to O3 compared to tall cultivar having lower yield potential. The shifting of crop calendar to bypass the peak concentration of O3 exposure to wheat was not effective, as delay in sowing time by 20 days decreased grain yield by 45.3% compared to timely sowing, which had only a 16.2% reduction (Ghosh et al., 2020).

In maize cultivars, elevated O3 (70 ppb) reduced the grain weight cob−1 in HQPM-1 by 5.8% and in PMH-1 by 11.3% compared to those at ambient concentration (Yadav et al., 2021c). Kernel weight m−2 and 1000 kernel weight declined more in DHM117 (normal maize) than HQPM-1 (quality protein maize) under exposure of elevated O3, suggesting greater susceptibility of DHM117 (Singh et al., 2019). The greater reduction in yield of DHM117 was contributed due to more depletion of carbohydrate content than HQPM-1 (Table 2).

Two soybean cultivars, PK472 and Bragg, were assessed for their response under elevated O3 and yield reduction was 20% and 33.6% in newly developed variety (PK472) while old variety (Bragg) showed reduction of 12% and 30% under 70 and 100 ppb O3 treatment, respectively (Singh et al., 2010a). Some other economically important crops of IGP also showed sensitivity under prevailing O3 stress. Singh et al. (2013) reported decrement in seed yield ranging between 22.7 and 26.2% under elevated O3 in Pusa Tarak cultivar of mustard (Brassica juncea L.). In an analysis on elevated O3 exposure and yield response of six mung bean cultivars, Chaudhary and Agrawal (2015) found that weight of seeds was reduced maximally in HUM-1 by 15.4% and minimally in HUM-23 by 9.8% (Table 2). Recently, an O3-FACE experiment based study also recorded losses in yield and harvest index of Chickpea (Cicer arietinum L.), a pulse crop by 21.9% and 36.10%, respectively at 60 ppb O3 concentration (Singh et al., 2021).

Horticultural crops are essential food as they provide necessary nutrients, minerals, and vitamins to human beings. India is ranked second in terms of horticultural crop production (Rais & Sheoran, 2015). Suganthy and Udayasoorian (2020) assessed the impact of elevated concentration of surface O3 at high altitude of Western Ghat on ten potato (Solanum tuberosum L.) cultivars at tuber initiation stage. The reduction in yield ranged from 4.56 to 25.5% with Kufri Surya to be moderately resistant to O3 with highest yield (Table 2). Both ambient and elevated levels of O3 detrimentally affected the yield of Kufri chandramukhi cultivar of potato owing to declines in weight and number of tubers (sizes > 35 mm) (Kumari & Agrawal, 2014). A study on tomato (Solanum lycopersicum L.) depicted that elevated O3 caused maximum reduction in yield during late vegetative phase (45 days old plant) than early vegetative and fruiting phases (Mina et al., 2010). Among leafy green vegetables, Palak (Beta vulgaris L.) is largely grown in suburban regions of India due to its high content of iron and folic acid and found to be extremely susceptible to O3 (Tiwari et al., 2010). Response of Palak to O3 was studied by Kumari et al. (2013) and 25% loss in yield was recorded (Table 2). Recently, Yadav et al. (2020b) screened forty Amaranthus hypochondriacus L. cultivars under FACE facility. Cultivars IC-5569 (91.4%) and IC-4200 (94.9%) showed very high decline in yield, while IC-5527 (7.8%) exhibited lowest yield loss.

Observation-based studies

An investigation of effects of surface O3 concentrations in Delhi revealed relative yield loss (RYL) of 7.5%, 5.4%, and 1.8% in the winter season and 22.7%, 16.3%, and 5.5% in the pre-monsoon season for wheat, soybean, and rice, respectively over a 7-year period (1997–2004) (Ghude et al., 2008). Another observation-based evaluation of 17 sites from India between 2011 and 2014 reported 4.2 to 15% annual yield loss in wheat and 0.3 to 6.3% in rice due to tropospheric O3 (Lal et al., 2017). Based on in situ O3 measurements for 2-year period (2011–2013) in Punjab and Haryana region of India reported that yield losses in wheat ranged between 27 and 41%, maize between 3 and 5%, and rice between 21 and 26% (Sinha et al., 2015). A recent study by Feng et al. (2022) has reported the RYL of 33%, 9%, and 23% for wheat, maize, and rice, respectively in China which is ~ US $63 billion in terms of annual economic loss.

A detailed analysis of O3 exposure based yield losses in the IGP region from 2010 to 2015 revealed losses of 1–5% at M7 (7-h mean O3 concentration) and 6–15% at AOT40 in wheat, and 0.3–0.7% at M7 and 7.2–7.5% at AOT40 in rice (Kumari et al., 2020). The RYL ranged from 10–34% for wheat, and 7–10% for rice based on AOT40, while under M7, RYL for wheat ranged from 3 to 11% and for rice from 0.7 to 4% (Kumari et al., 2021). Osborne et al. (2016) gathered O3 exposure yield related data (1998–2014) of 49 soybean cultivars from around the world at M7 of 55 ppb and discovered that Indian cultivars (which lost yield by 38%) are more susceptible to O3 than cultivars from China and the USA.

Model-based studies

A study by Van Dingenen et al. (2009) assessed the impact of tropospheric O3 on crops using global-scale modelling and predicted the annual yield loss for wheat ranging between 13 and 28% and for rice between 6 and 8% in India. Weather Research and Forecasting model coupled with Chemistry (WRF-Chem model) estimated 3.5 ± 0.8% losses in wheat and 2.1 ± 0.8 losses in rice, with maximum losses occurring in central and north India (Ghude et al., 2014). Recently, Sharma et al. (2019) reanalyzed the yield loss in India using the WRF-Chem model and found 21% and 6% yield losses in wheat and rice, respectively, which are considerably higher than previous studies (Table 2). An analysis of 2-year data based on O3-flux model on four Indian wheat cultivars depicted that the loss in grain yield was higher (23.9% ± 1.35) in early sown cultivars compared to late sown cultivars (11.5% ± 0.37) under ambient + 20 ppb O3 (Yadav et al., 2021a).

EDU as a research tool in estimating the yield losses against O3

Ethylene diurea (EDU; [N-(2–2-oxo-1-imidazolidinyl) ethyl]-N-phenyl urea) is a well-known antiozonant research tool that was first described by Carnahan et al. (1978). Due to its phytoprotective responses, it is widely used for screening the cultivar’s specific sensitivity, and assessing losses in yield under ambient and elevated O3 conditions (Singh et al., 2015b). Application of EDU as control in comparison to ambient O3 is beneficial for adequate monitoring of effects of ambient O3 on agricultural crops in rural areas of India with electricity limitations (Manning et al., 2011; Tiwari et al., 2005). In India, several experiments using EDU as protectant to O3 have been investigated for determining the variability among cultivars in terms of improvement in yield such as for wheat (Singh et al., 2009b), rice (Pandey et al., 2015), mustard (Pandey et al., 2014), and soybean (Singh & Agrawal, 2011a) (Table 3).

Table 3 Yield response of ozone exposed plants upon EDU treatment
Full size table

Recently, Mina et al. (2021) assessed the responses of thermotolerant wheat cv. WR544 to O3 by applying 300 ppm EDU and found that harvest index was higher in EDU treated plants (37.4%) as compared to non-treated plant. Another study on three wheat cultivars by Fatima et al. (2019) found that EDU treatment (300 ppm) increased yield of HD 2987 (O3 sensitive) by 32.9%, PBW 502 (intermediately sensitive) by 13.3%, and Kharchiya 65 (O3 tolerant) by 8.8% (Table 3). Similarly in two rice cultivars, PB-1 (O3 sensitive) showed about 25% increase in seed weight plant−1 in EDU treated plants than Sarjoo-52 (O3 tolerant) which showed lower increment of 8.9% (Surabhi et al., 2020). Application of 50 and 200 ppm EDU on two maize cultivars showed protection by enhancing anti-oxidative defence machinery, ultimately greater yield in SHM3031 (sensitive variety) as compared to PEHM5 (tolerant variety) in response to high O3 concentration (Gupta et al., 2020). A similar finding was also observed for the maize cultivars Buland and Prakash with 200 ppm EDU doses under ambient and elevated O3 (Singh et al., 2018a).

The exact mode of action of phytoprotection provided by EDU against O3 induced damage has remained unclear till now. An expected mechanism has been ascribed to its capability to induce enzymatic and non-enzymatic antioxidants which detoxify ROS (Pandey et al., 2015; Singh et al., 2018a). Agathokleous (2017) in its review gave another view of perception towards the phytoprotective mechanism of EDU by showing hormetic (means activating plant defense at a low stress dose) responses against ambient and elevated O3 stress. There are several evidences that showed hormesis in a plant species by using low doses of abiotic agents like O3 or specific chemicals such as EDU (Agathokleous & Kitao, 2018; Agathokleous et al., 2019; Calabrese & Blain, 2011). The EDU mediated hormetic responses were measured in various endpoints such as growth, physiology, reproduction, and productivity (Agathokleous & Kitao, 2018; Agathokleous et al., 2019). Dose response study manifested that treatment of EDU (0–800 mg·L−1) induced hormesis in radish (Rapahanus sativus L.) plant (by stimulating fresh weight of cotyledons and dry weight of root) placed in nonfiltered air receiving ≈25 ppb O3 concentration, and the maximum stimulation was recorded at 300 mg L−1 (Agathokleous, 2017; Kostka-Rick & Manning, 1993). Another experiment with carrot (Daucus carota L.) grown in ambient O3 concentration on treatment with EDU (0–450 mg L−1) mediated hormetic responses in terms of growth and nutritional aspect, and the highest immensity of positive response was recorded at 150 mg L−1 (Tiwari & Agrawal, 2010). Earlier, an EDU-mediated hormetic response has also been reported in wheat (Archambault et al., 2002). Further, it is shown that conditioning may be an important aspect of hormesis and O3 may activate conditioning in plant defense strategy (Sandermann et al., 1998). Preconditioning of tomato calli with 100, 200, or 300 ppb O3 for 7 days (30 min d−1) induced resistance in regenerated plantlets towards O3 exposure (200 ppb, 2 h) by altering the antioxidant potential (Nagendra-Prasad et al., 2008). Similarly, Li et al. (2017) also showed such response in bean (Phaseolus vulgaris L.) plants on pretreatment of O3 (≈200 ppb for 30 min), which prevented against more extensive exposure to O3 (600 ppb for 30 min).

Nitrogen fertilization in alleviating the impact of tropospheric O3 on crops and vegetables

Inorganic nitrogen (N) fertilizers are widely used to increase grain production (Akhtar et al., 2020). There have been a lot of studies done on the connection between elevated O3 and nitrogen management, but the obtained results were variable (Feng et al., 2019). Singh et al. (2015a) found an antagonistic response where a high dose of N mitigated the negative response of O3 stress on wheat plants. At recommended NPK (RNPK), mustard cultivars Vardan and Aashirwad, which were grown in non-filtered chambers (NFCs) receiving ambient O3, had significant drops in their micronutrient, protein, and seed oil contents. But at 1.5-times the RNPK, they did not have significant changes (Singh et al., 2012). In a study on interactive effects of different concentrations of N and elevated O3 on wheat cultivars, HD2967 and Sonalika showed differential responses (Pandey et al., 2018). In Sonalika, treatment with a high dose of N did not alleviate the O3 phytotoxicity in relation to yield, while HD2967 showed alleviation (Pandey et al., 2018).

Another study by Singh et al. (2015a) with LOK-1 and HUW 510 cultivars of wheat depicted that ambient O3 negatively affected the N acquisition, which increased the demand of N in sensitive cultivar LOK-1 and hence increase in yield was recorded at 1.5-times recommended N dose (Table 4). However, HUW 510, being less sensitive, showed an increase in yield under ambient O3 at recommended N. Similarly, Gautam et al. (2020) found that 1.5-times recommended dose of N was sufficient to relieve the negative impact of ambient O3 on maize cultivars (Malviya hybrid-2 and HHM-1) by enhancing crop productivity, while 2-times recommended dose of N did not provide any additional benefit to plant metabolism compared to 1.5 times N dose (Table 4). Further, differences in allocation strategies during developmental phases led to greater increment in yield of Malviya hybrid-2 than HHM-1. Under ambient O3 conditions, N amendments (in the form of NPK) induced antioxidant defense machinery in a more competent manner in tolerant cultivar (PUSA-N) of Cluster bean (Cymopsis tetragonoloba L.) compared to sensitive cultivar (S-151), which showed decline in stomatal conductance as an avoidance strategy (Gupta & Tiwari, 2020). An experiment on Palak (Beta vulgaris L.) also found that adding nitrogen to the soil helped to lessen the effects of O3 stress by changing the plant’s antioxidative properties (Sahoo & Tiwari, 2021).

Table 4 Responses of plants tropospheric O3 under N fertilization
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The possible mechanism of alleviation of O3 toxicity under N supplementation relies on positive impact of N on photochemical processes followed by increased carbon assimilation rate. This type of reaction could be linked to the expenditure of available N in protein, which may enhance the photosynthetic ability (Singh et al., 2015a). The proteins are important factors for defense machinery and, hence, N addition alleviates O3 phytotoxicity (Yendrek et al., 2013). Insufficient N fertilization restricts the photosynthetic N use efficiency, which declines the grain yield. However, optimum N addition enhances the grain yield (Singh et al., 2015a).

The beneficial role of nitrogen on performance of plants exposed to O3 can also be assigned to upregulation of enzyme activities of Halliwell-Asada pathway (APX, ASA, and DHA) under nitrogen implementation (Fig. 1B; Gupta & Tiwari, 2020; Pandey et al., 2018). Elevated O3 exposure led to decline in seed protein in soybean, which is correlated with a detrimental reaction to nitrogen fixation (Broberg et al., 2020). It is also shown in rice that elevated O3 treatment declines the nitrate reductase (NR) activity, NH4+-N and NO3−-N contents (Fig. 1A; Huang et al., 2012). So, implementation of N may trigger N metabolism and may alter the allocation of N towards structural proteins and photosynthesis (Liu et al., 2018). Under O3 stress, application of high dose of nitrogen delayed the leaf senescence process by conserving high protein content (Pandey et al., 2018).

Fig. 1
figure 1

Schematic representation illustrating A) the impact of elevated O3 on nitrogen metabolism and yield reduction, and B) role of nitrogen addition in combating harmful effect of tropospheric O3 on plants. Nitrogen addition scavenges O3 induced reactive oxygen species by upregulating antioxidative and Halliwell-Asada pathway enzymes. Contrarily, nitrogen addition mediated the carbon pool partitioning away from sucrose synthesis by deactivating SPS and being assisted towards amino acid synthesis by activating PEPcase. GS, glutamine synthetase; GOGAT, glutamine oxoglutarate aminotransferase; SPS, sucrose phosphate synthase; PEPcase, phosphoenolpyruvate carboxylase; PK, pyruvate kinase; PEP, phosphoenolpyruvate, OAA, oxaloacetic acid. Pointed arrow end represents induction and blunt end represents inhibition. Enhancements in parameters are shown by ↑ and reduction by ↓

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It is observed that the biosynthetic pathways of sucrose and amino acids compete for energy and carbon skeleton (Champigny & Foyer, 1992). A study on effect of nitrate on wheat seedlings showed an inverse response between the rate of sucrose formation and the assimilation rate of NO3− (Van Quy et al., 1991). The two key enzymes, sucrose phosphate synthase (SPS) and phosphoenolpyruvate carboxylase (PEPcase), are responsible for carbon assimilation partitioning, and are modified by protein phosphorylation under nitrogen addition. But the reactions of both the enzymes show the opposite trend. Application of nitrogen reduces the content of PEP and activates PEPcase in leaves, which is linked to increased carbon flux towards amino acids (Fig. 1B). Accordingly, decrement in SPS activity restricts the synthesis of sucrose in leaves, suggesting that SPS plays a major role in flux of carbon towards sucrose (Champigny & Foyer, 1992). Although, in our understanding, there are very few studies indicating mechanism of carbon partitioning in crops and vegetables, which needs to be explored in future to assess the exact mechanism of nitrogen supplementation in alleviating O3 stress.

Conclusions and future prospects

The present compilations of data on Indian agricultural crops clearly highlight the crop’s sensitivity to present and future levels of O3, experiencing significant yield losses. Ozone pollution is worsening and heavily impacting the crop’s productivity, thus posing a threat to food security in near future. Cumulative stress response index, phytotoxic O3 dose, and foliar injury are some important tools for estimating the sensitivity of crops against O3 stress. The studies clearly indicate that wheat is the most sensitive crop to O3 and hence showed greater loss in yield than rice. Maize is found to be less sensitive to O3 in IGP region under present O3 scenario. The sequence of susceptibility of major crops is wheat ˃ mustard > rice > maize in IGP region. Under high O3 concentration, Ethylenediurea (EDU), an O3-protectant, is beneficial to evaluate crop yield losses in remote areas where electricity and infrastructures are limited. Implementation of N fertilizers (1.5 times the recommended NPK) effectively ameliorated the loss in grain yield under ambient and elevated O3 by activating antioxidative pathway.

Taking into consideration the vulnerability of economically important crops and vegetables in India to elevated surface O3 concentration, mitigation perspective should be taken to reduce emission of O3 precursors. In European Union and United States of America, various strategies and implementation plans such as European Crop Loss Assessment Network (EUCLAN) and National Crop Loss Assessment Network (NCLAN) program were initiated and implemented, which effectively led to decline in O3 concentrations. Such network programs are needed in India to assess the countrywide yield losses. Ozone biomonitoring and assessment programs may also include O3-sensitive common biomonitors such as clover NC-S, snap bean genotype S156, and tobacco cultivar Bel-W3 to recognize air quality and climatic conditions in a specific region. Recently, some biomonitoring concepts such as O3-Gardens of ICP Vegetation and the O3-Bioindicator Garden Project of NASA were introduced for creating gardens having O3 sensitive and resistant varieties of plants and raising public awareness of the threats posed by tropospheric O3 across the region. Such awareness programs must be initiated by other countries at local and large scale.

In India, one of the biggest issues is the inadequate monitoring setup in rural areas that should be strengthened to provide accurate data regarding O3 concentration. The accessibility of EDU chemical should be promoted in rural areas for cost-effective short-term O3 biomonitoring and also for identifying indicator plant species against ambient O3 in natural habitat.

Solar radiation, drought, temperature, and CO2 are major factors that directly or indirectly modulate the effects of elevated O3 on plants. These interactions need detailed analyses under various cropping pattern in the future. Therefore, O3-flux-based metrics should be considered over the exposure-based metrics by the researchers for precise O3 risk assessment and flux-response functions. The impact of elevated O3 on plants differs with the addition of nitrogen as a fertilizer. Therefore, more studies on responses of crops and vegetables after implementation of an appropriate dose of nitrogen under O3 stress should be promoted to understand the exact mechanism of plants. Use of beneficial agricultural practices in ameliorating the negative impact of tropospheric O3 on productivity of crops could be worked out in future.

It is evident that to reduce yield losses, O3 tolerant cultivars should be encouraged in future to withstand O3 stress condition. Therefore, different cultivars of crops and unexplored cultivars need to be screened for their tolerance and sensitivity to O3. Biotechnological tools and conventional breeding approaches are required to produce O3 tolerant cultivars by modifying antioxidant defense pathways, stress regulated genes, and signaling pathways, which may be beneficial to restrict yield losses due to elevated O3 in future.