1 Introduction

Tropospheric ozone (O3), a critical greenhouse gas, strong oxidant, and secondary gaseous pollutant, has been held responsible for adversely impacting human well-being [1]. Rising O3 levels have been attributed to 4.14 million premature deaths and a loss of 118 million disability-adjusted life-years (DALYs) globally in 2019 [2]. It has estimated to impose a substantial impact on global crop productivity leading to a loss of 63 billion US $ [3]. In the recent air quality guidelines (AQG), the World Health Organization (WHO) has set 50 ppb as the 99th percentile of daily maximum 8-h O3 concentration for the safeguarding of human health [4]. Other air quality matrices in India viz. National Ambient Air Quality Standards (NAAQS) adopted in 2009 has revised the national standards for 8-h daily maximum ground level O3 at 50 ppb, similar for industrial, residential, rural, and ecologically sensitive areas. It is set at 92 ppb for 1 h daily maximum for the same areas mentioned in the former [5].

Major adversities of tropospheric O3 on the plants range from yield reduction [6] to decline in biomass [7, 8]. It has been projected that O3 can be more dangerous to global food security than climate change [9]. For protecting vegetation, the most widely used index for accumulated hourly O3 concentrations above 40 ppb over daylight hours during the growing season, is AOT 40 (Accumulated Ozone exposure over a Threshold of 40 ppb) [10]. O3 enters the plants through stomata during the gas exchange process, and post its uptake, O3 is rapidly dissolved in the apoplastic region, levying the plants with oxidative stress, leading to an imbalance in the cellular redox state and eventually causing cellular damage or death [11, 12]. This apoplastic oxidative stress triggers lipid peroxidation and causes visible symptoms in the plants as necrotic spots [13]. Such structural injury in turn affects the physiology (stomatal conductance and assimilation rate) and biochemistry (photosynthetic pigments, enzymes and antioxidants) of the plants, eventually dismantling the partitioning of photosynthates to sink. These responses cause alterations in metabolism of the exposed plants which further reduces plant growth rate, crop production, nutritional quality and above- and below-ground biomass [14, 15].

Northern India encompasses one of the world's most fertile regions- the Indo-Gangetic Plains (IGP), also known as India's ‘food basket’ because of its high crop productivity. It is also the densely populated region of India, and the population corresponds to its higher pollution load, making it a ‘hot spot’ of air pollution [16]. Tropospheric O3 is one of this region's major air pollutants responsible for a significant decline in crop yield. According to modeling projections, the loss of global primary productivity (GPP) due to O3 is expected to grow significantly [17]. Across the majority of the 37 European locations, GPP is favorably correlated with O3 fluxes and negatively correlated with O3 concentrations and GPP is negatively impacted by O3 to the extent of 30%, with varying degrees of impact across plant functional types in Europe. It is also predicted by global photochemical models that portions of Asia, including India, will experience further considerable rises in O3 concentrations by 2030 [18]. By 2100, for all Representative Concentration Pathways (RCPs) the ozone hotspots (> 50 ppb and AOT > 70 ppm h) are in Southern Asia. For RCP2.6 and RCP4.5, small reduction in surface ozone levels in southern and eastern Asia highlight the small changes in ozone precursor emissions due to the recent emission growth in this region. For RCP8.5, the high O3 increase (up to 10 ppb) in southern Asia can be attributed to substantial increase in CH4 emissions coupled with a strong global warming, exceeding 2 ℃, and a weakened NO titration and a greater stratospheric O3 influx [19]. Recent studies have reported the adverse effect of tropospheric O3 on crops (both agricultural and horticultural) in terms of their productivity [20,21,22,23,24,25,26]. However, a literature gap is still observed for the studies focusing on the mechanistic responses and trade-off strategies observed in the plants exposed to O3 stress. The present review aims—to (1) assess the response of Indian vegetation (major crops and perennial plants) in terms of yield, quality, and productivity under the elevated O3 (EO3) stress for past 11 years, (2) target the major mechanism behind the observed responses and ultimately categorizing them based on their mechanism of response against the futuristic O3 concentration.

2 Diurnal ozone atmospheric chemistry and meteorological influences

The formation of ground-level O3 might involves stratospheric influx [27, 28] or generated by photochemical reactions of air pollutants like nitrogen oxides (NOx) and volatile organic compounds (VOCs) in the troposphere (Fig. 1). The spatial distribution of O3 depends on (1) the balance between photochemical formation and destruction of O3, (2) the prevalent meteorological conditions of the area, (3) physical processes regulating hemispheric transport and removal of O3 by deposition, (4) propinquity to the sources of precursor gaseous pollutants, and (5) geographical location and topology of the area [24], etc. The formation of photochemical O3 takes place during the day, peaking at midday, and then gradually declines with a reduction in solar irradiance (Fig. 1). Following sunset, NO titration causes a decline in the O3 concentration, which reaches its lowest level in the late night or early morning [29].

Fig. 1
figure 1

Illustration of O3 atmospheric chemistry during day and night. The upward triangle represents an increase in O3 formation during the day, and the inward shows a decrease in O3 formation during night

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3 Effect of ozone on the yield and productivity

Various field experiments in near-natural conditions using open-top chambers (OTCs) carried out in IGP have evaluated the productivity losses and quality degradation in important crops and vegetables caused by present and projected O3 concentrations [26, 30]. Different cultivars of the crops experienced variations in the immensity of yield reduction, which is mainly ascribed to the innate plant characteristics, differential assimilate translocation to reproductive parts and grain filling, visible foliar injury, variable reductions in photosynthesis and stomatal conductance, and enhanced loss of metabolic energy in the antioxidant defense system (Table 1). The mechanistic approach behind the reduction in yield and biomass of different vegetation is given below:

Table 1 Details of ozone induced responses in studies
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3.1 Effects on agricultural crops

Rice is the most important cereal in Asia, especially in India and Southeast Asia. Reduction in rice yield due to surface O3 ranges between 7 and 13% in the northern region of India [31] (Table 1). Recently, a study focusing on fifteen rice cultivars revealed that EO3 reduced the photosynthetic characteristics, tiller numbers, and rise in spikelet sterility, leading to yield loss in all the cultivars with varying magnitude [32]. It is manifested that O3 exposure declines photosynthate allocation to panicles to enhance antioxidant metabolism and plant respiration.

In India, wheat is the second most important crop after rice, and O3 also causes a reduction in its yield, ranging between 11 and 20.7% in IGP [31]. According to several reports, different wheat cultivars showed different strategies to overcome yield reduction under O3 stress condition (Table 1). Recently, significant reduction in grain production in HUW468 and HD3086 (30.5%) (early sown wheat cultivars) than in HUW234 and HD3118 (21.3%) (late sown wheat cultivars) was mainly attributed to greater stomatal uptake throughout the experimental period and longer life span [33]. The same study also observed the O3 flux effect relationship through the DO3SE (Deposition of Ozone for Stomatal Exchange) model. It depicted that for a 5% reduction in yield in the early sown cultivars, the critical level of Species-specific phytotoxic O3 dose above a threshold of 6 nmol m2 PLA s−1 (POD6SPEC) was 0.284 mmol O3 m−2 and found to be lower than late sown cultivars (0.393 mmol O3 m−2). As the critical condition occurs at a lower concentration of POD6, this shows that early-sown cultivars are more susceptible to O3 than late-sown cultivars. Additionally, it has been found that early-sown cultivars consume more metabolic energy than late-sown cultivars to create enzymatic and non-enzymatic antioxidants against higher O3, which may partly explain their higher reduction in yield [34]. Elevated O3 reduced grain yield significantly in the modern wheat cultivar (23.8%) than the old cultivar (22.1%) due to enhanced stomatal density and correspondingly higher conductance in the modern wheat cultivar resulting in greater O3 uptake, which led to a higher decline in photosynthetic pigment along with a reduction in photosynthetic rate and photosynthetic nitrogen use efficiency (PNUE) ultimately causing more yield losses [35] (Fig. 2). Moreover, a decrease in flour quality was also evident in the modern cultivar under due to increased protein loss and decreased levels of important amino acids EO3 treatment.

Fig.2
figure 2

A comparative analysis of field studies conducted to assess O3 induced yield losses under ambient and elevated O3 concentrations. Symbols represent mean with range of yield loss at elevated O3 concentrations

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Ghosh et al. [36] reported that delayed sowing of HD 2967 wheat cultivar and EO3 have been found to have a synergistically detrimental effect on yield (45.3%) as compared to ambient O3 and timely sown condition (Fig. 2). The increased yield loss in the late sown wheat cultivar under EO3 was attributed to a shorter growth period, reduced photosynthetic rate, improper assimilation of photosynthates, and enhanced AOT40 value during the grain filling stage while timely sown plant comparatively experienced lower AOT40 value leading to a lesser reduction in its yield. Another study revealed that O3 sensitive (HD 2987) wheat cultivar experienced greater oxidative stress and tried to combat it by boosting the enzymatic antioxidants, salicylic acid and enzymes of the phenylpropanoid pathway and thus maximized the losses in reproductive structure and yield than PBW 502 (intermediately O3 sensitive) and Kharchiya 65 (O3 tolerant) [37]. However, in PBW 502 both non-enzymatic and enzymatic antioxidants were increased while in Kharchiya 65, induction of total thiol, reduced glutathione (GSH), ascorbic acid, jasmonic acid and radical scavenging activities contributed efficiently to alleviate O3 stress. The antioxidants (thiols and ascorbic acid) and yield responses to EO3 were studied for fourteen Indian wheat cultivars, revealing higher upregulation of both the antioxidants and its ratio in the O3 resistant category, followed by moderately O3 sensitive and least in the O3 sensitive category [38]. More yield losses were observed in the O3-sensitive wheat cultivars, due to greater reactive oxygen species (ROS) induced damage and minimum increment in ascorbic acid, thiol and its ratio, implying them to be potential biomarkers for O3 tolerance.

Another study reported that Triticum aestivum L. (modern and popular wheat species) showed a greater reduction (17%) in yield than an older species, T. durum (11%) under EO3 exposure [39]. The decline in the yield of wheat was attributed to a significant reduction in the photosynthetic rate, stomatal conductance, and carbon fixation, resulting in less accumulation of dry matter and enhanced leaf senescence, which was further responsible for the lowered grain filling period and eventually decreased yield. Additionally, decreased photosynthesis also results in a significant drop in the amount of carbohydrate (starch and sugar) content because less is translocated to grains. Similarly, Mishra et al. [40] manifested a reduction of 39% in the yield of HUW-37 (dwarf wheat) compared to 12.4% in K-9107 (tall wheat cultivar) because of the negative impact on growth attributes and lesser biomass accumulation and translocation of photosynthates to reproductive parts.

Major commercially important leguminous crops showed differential mechanisms of yield reduction to the prevailing O3 stress (Table 1). Under EO3 exposure, alterations in plant's physiological, biochemical, growth, and yield properties varied considerably in eight black gram (Vigna mungo L.) varieties [41]. The cultivar VBN3 (most O3 sensitive) displayed greater yield loss due to their higher leaf injury percentage and malondialdehyde (MDA) content, causing prolonged stomatal closure and decreased carbon fixation ability and availability of assimilates for yield. In contrast, VBN8 (most O3 resistant) exhibited relatively higher physiological performance and yield than other varieties, associated with higher ascorbic acid content, minimum leaf injury percentage and MDA content.

Mishra and Agrawal [42] observed the differential response of two mung bean cultivars- HUM6 and HUM2, to EO3 and established that HUM-2 suffered more damage and reduced quantum yield than HUM-6. This decline was due to increased ROS induction and foliar injury, along with a decline in the RuBisCO protein and decreased ability of HUM-2 to produce enough antioxidants. Chaudhary et al. [43] reached a similar conclusion while studying the response of six mung bean cultivars to EO3. The degree of foliar injury correlates with the sensitivity of the cultivars to the applied O3 stress. Cultivar HUM1 with maximum foliar injury displayed a decrease in chlorophyll content and photosynthetic rate due to stomatal closure accompanied by a decline in biomass, indicating its higher susceptibility to O3 than the other cultivar. A higher decline in the growth and yield, in addition to lower induction of enzymatic antioxidants, also illustrated the intensive sensitivity of cultivar HUM-1 towards O3, while HUM-23 showed greater O3 tolerance by exhibiting strong antioxidative defense machinery impeding minimum yield reduction [44]. Elevated O3 also reduced the starch, soluble sugar, and protein contents in the seeds of all the cultivars, which correlated with decreased photosynthesis and limited translocation to reproductive parts.

Maize (Zea mays L.) is one of the most consumed food crops in the world after rice and wheat. It is a rich source of vitamins A, B, and E, as well as several minerals and its oil is most qualitative among the edible oils due to the large amount of unsaturated fatty acids (oleic and linoleic acids). Yadav et al. [45] assessed the impact of EO3 on two maize cultivars, HQPM-1 and PMH-1 and reported a reduction in the yield (HQPM-1 (9.2%) and PMH-1 (9.8%) (Fig. 2). A similar study, with variable doses of EO3 on two maize cultivars, HQPM-1 and DHM117, also reported a reduction in yield with a maximum reduction of 14.7% in the DHM117 cultivar [46]. Both studies concluded that yield reduction was due to a significant decline in the photosynthetic rate and stomatal conductance of PMH-1 and DHM117. The EO3 concentration not only negatively affected the yield but significantly modified the nutritional parameters of maize seeds [46]. Parameters like crude protein content, total soluble sugar, reducing sugar, and elements like Ca, Fe, and Mg increased under EO3 in both the maize cultivars, where maximum increment was found in HQPM-1 cultivar. At the same time, other nutritional parameters such as starch content, essential amino acids (tryptophan and lysine), and mineral elements like P, Na, and K were negatively affected under EO3, along with the oil content and quality in both the cultivars. However, a contrasting result of the reduction in oil yield was found whereby maximum oil yield loss occurred in HQPM-1.

India's third-most essential oil crop is the rape seed mustard (Brassica species), which roughly accounts for 20–25% of all oilseed production [47]. A study on Brassica juncea L. revealed that EO3 decreased its yield due to a decline in leaf area index and photosynthesis [48] (Table 1). The nutritional quality of seeds also deteriorated along with the yield loss by O3 stress, mainly the reductions in oil content, protein, and micro and macronutrients. Tripathi and Agrawal [49] studied two cultivars of Indian mustard (Sanjukta and Vardan) and showed cultivar-specific responses of EO3 exposure, with Sanjukta displaying a greater decline in photosynthetic traits, reproductive structures, oil, and seed quality, whereas in Vardan yield was adversely impacted. It manifested the correlation between O3-induced alteration in photosynthetic attributes, growth of reproductive tissues, and the final yield; however, B. campestris L. did not demonstrate compensation for loss occurring at the vegetative and reproductive stages to the economic yield. Alterations in the fatty acid profile and reduced oil and protein contents were observed under EO3 in both Vardan and Sanjukta [49]. The increased amount of PUFA, o-6 fatty acids, erucic acid, and linolenic acid in the oil decreased its oxidative stability under O3 exposure, indicating a deterioration of the oil quality of the test cultivars [49].

3.2 Effect on horticultural crops

Vegetable crops are crucial food sources because of abundance of necessary vitamins, minerals, and other nutritional substances for human health. According to Rais and Sheoran [50], India is the second-largest producer of horticulture crops. Suganthy and Udayasoorian [51] observed the effect of variable concentrations of EO3 (100 ppb, 150 ppb, and 200 ppb) on ten cultivars of potato (Solanum tuberosum L.) at the tuber initiation stage. The yield reduction ranged from 4.6% to 25.5%, with a minimum reduction in Kufri Surya, showing moderate resistance against EO3. In a study on Solanum tuberosum cultivar Kurfi Chandramukhi (early maturing variety) by Kumari and Agrawal [52] observed significant reduction in the yield and quality of tubers under both ambient and EO3 (Fig. 2). It adversely affected the photoassimilate partitioning to belowground parts, reducing the biomass of tubers. Intermediate (35–50 mm) and large sized (> 50 mm) tubers were reduced at the harvest stage leading to higher economic loss. Another study was conducted to assess the impact of EO3 on eight cultivars of tomato (Solanum lycopersicum L.) having differential sensitivity towards heat by Gupta et al. [53]. The study reported reduction in yield that ranged between 11.5 to 41.6%, with Kashi Chayan and VRT02 being resistant cultivars with minimum yield loss, whereas Superbug and Sel7 cultivars were sensitive with maximum yield loss [53] (Fig. 2). The reduction in yield of sensitive cultivars was attributed to the decline in photosynthesis, stomatal conductance, and higher input of non-enzymatic antioxidants in alleviating the harmful effects of O3 rather than investing in reproduction. Singh et al. [54] evaluated the effect of EO3 on three Abelmoschus sp, with different levels of ploidy, namely, A. moschatus (monoploid), A. esculentus (Diploid) and A. caillei (triploid). They reported a maximum reduction in the yield in A. moschatus (29.2%) attributed to the lower induction of enzymatic antioxidants and higher energy investment in producing non-enzymatic antioxidants (Fig. 2).

Beta vulgaris L., (leafy green vegetable) is widely cultivated in suburban areas of India because of its high nutritional value (a rich source of folic acid and iron). Kumari et al. [55] evaluated the response of B. vulgaris to O3 and reported 41.2% decline in the yield along with a degradation in nutrient quality under the applied stress. The O3 induced reduction in the photosynthetic activity of plants and a higher allocation of photoassimilates towards defense ultimately lead to yield reduction (Fig. 2). In another study, forty cultivars of Amaranthus hypochondriacus L. were screened for their varied responses to surface O3 using the FACE facility [56]. It was concluded from the study that the cultivar IC-5527 showed the lowest yield reduction of 7.8%, whereas cultivars IC-5569 and IC-4200 exhibited a decline of 91.4% and 94.9% in yield, respectively (Fig. 2).

The effect of surface O3 has also been studied on a few economically important crops in India. Groundnut (Arachis hypogea L.) is one of the significant leguminous crops, farmed mainly for the edible oil extracted from its seeds. India is the second largest producer of groundnut in the Asian continent. Chaudhary and Rathore [57] assessed the impact of EO3 on the Arachis hypogea cultivar TG-37 and showed a maximum yield reduction of 53.97%. In contrast, cultivar TAG-24 depicting a minimum yield loss of 7.56%. It is inferred that the yield reduction was a cumulative effect of impaired plant physiological activities in response to EO3 along with the varied genetic makeup of the cultivar (Fig. 2). In another study, Chaudhary and Rathore [58] analyzed the effect of O3 on the five Gossypium hirsutum L. (cotton) cultivars and reported that among the studied cultivars, ADC-1 is highly susceptible while V-797 is resistant to the applied stress. Elevated O3 also affected starch and protein contents. The reduction in the yield and quality parameters possibly occurred due to greater allocation of photosynthates towards the below-ground parts of the plants.

3.3 Effects on medicinal plants

India has been a hub of medicinal plants since pre-historic times, and hence are well explored for their therapeutic and pharmaceutical properties. The effect of O3 on medicinal plants has been assessed by a few Indian workers [59, 60] (Table 1). An anti-diabetic perennial herb, Costus pictus D. Don showed a significant reduction in leaf area and total plant biomass when fumigated with 20 ppb of O3 [59] (Fig. 3). An increase in lipid peroxidation and solute membrane leakage further intensified the foliar injury. Leaves and rhizomes of the plant showed an overall increase in the production of secondary metabolites such as alkaloids, tannins, lignin, and saponins, along with a major bioactive compound, i.e., corosolic acid, under EO3. The increase in enzymatic antioxidants helped to efficiently detoxify the higher ROS level, while the enhanced non-enzymatic antioxidants act as a shield for chlorophyll molecules. Ansari et al. [61] found reductions in growth parameters, root shoot ratio, and biomass in Sida cordifolia L. under an EO3 exposure of 20 ppb (Fig. 3). Most reproductive parameters, also responded negatively under O3 stress. However, the major metabolites (stigmasterol, B-sitosterol, squalene, and B-caryophyllene) were upregulated. The reductions in growth parameters supported the fact that plants utilize their assimilates toward defense against the O3 stress; hence, an increase in enzymatic and nonenzymatic antioxidants was observed. The production of several secondary metabolites, namely lignin, tannin, saponin, and alkaloids, was stimulated in the leaves and roots of Sida cordifolia, while the photosynthetic pigments and physiological parameters were decreased under O3 exposure. Further, the plants modified their leaf morphology by increasing their trichome density for better adaptation to O3 stress [62]. Similar results were reported by Madheshiya et al. [60] in a perennial grass, Cymbopogon flexuosus (Steud.) (Wats.), exposed under two elevated levels of O3 (AO3 + 15 ppb and + 30 ppb). An increase in enzymatic and nonenzymatic antioxidants helped in scavenging ROS at later growth stages. The biomass reduction with an increase in metabolites and essential oil content corroborated the allocation of resources more towards the phenylpropanoid pathway. Besides increasing the metabolite content, EO3 also formed new bioactive compounds (Fig. 3).

Fig. 3
figure 3

A comparative analysis of field studies conducted to assess O3- induced biomass losses under ambient and elevated O3 concentrations. Symbols represent mean with range of biomass reduction at elevated O3 concentrations

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3.4 Effects on perennial vegetation

An array of persistently adverse physiological and biochemical changes was evident in Leucaena leucocephala (Lam.) seedlings under an elevated exposure of 20 ppb of O3 in Free Air Ozone Enrichment (FAOE) [63] (Fig. 3). Reductions in photosynthesis, photosynthetic pigments, and lipid peroxidation were found throughout the exposure, while the stomatal conductance and transpiration rate were decreased after 12 months of exposure. Several enzymatic antioxidants (catalase, ascorbate peroxidase, and glutathione reductase) were increased after an exposure of 12 months. The plant showed more sensitivity during the initial exposure of 12 months but later developed tolerance by the end of the exposure period.

Jamal et al. [64] experimented with nine tropical tree species (Azadirachta indica A. Juss., Bougainvillea spectabilis Willd., Ficus benghalensis L., Ficus religiosa L., Nerium indicum Mill., Plumeria rubra L., Saraca asoca Roxb., Tabernaemontana divaricata a R. Br. ex Roem. & Schult and Terminalia arjuna Roxb.) exposed to EO3 in FAOE. Photosynthetic rate, stomatal conductance, and transpiration rates were reduced under EO3 in all the species except A. indica and N. indicum, where stomatal conductance was increased. A decrease in stomatal density and an increase in guard cell length was found in A. indica, B. spectabilis, P. rubra, S. asoca, T. divaricata, whereas a reverse response was observed in F. benghalensis and T. arjuna. Among all the tree species, S. asoca and F. religiosa were the most tolerant species, while B. spectabilis and A. indica were the most sensitive ones.

The implications of O3 on biomass and productivity of tropical tree species have not been much explored, and only a few studies have been conducted in Indo-Gangetic plains [65, 66]. The detrimental effect of O3 was reported by Singh et al. [66]on aboveground plant parts and belowground soil fertility. The study revealed the negative impact on shoot length, root, shoot, leaf, and total biomass under EO3 exposure. Reductions in extracellular enzymatic activities, microbial biomass carbon, nitrogen, and phosphorus were also found. Another study by Singh et al. [65] of productivity losses in two Indian hybrid varieties (Amrapali and Mallika) of Mangifera indica L. revealed a captivating resource allocation strategy between growth, subsistence, and productivity under EO3 exposure of 20 ppb. Elevated O3 affected the height-diameter allometry of both the varieties, thus leading to a significant increment in the plant height in the case of Amrapali at the expense of stem diameter, while Mallika showed a reverse response. Under the EO3 stress, yield parameters responded negatively in both varieties; hence, greater investment in growth parameters compromised the fruit-yielding properties of the plants.

3.5 Effect of ozone on the community level productivity of grasslands

In a study on grassland species, Dolker et al. [67] observed the effect of EO3 (Ambient + 30 ppb) on two tropical grass species (Panicum maximum Jacq. and Cenchrus ciliaris L.), which are common in IGP. There was a significant decline in both species' growth and biomass under the applied stress (Fig. 3). However, they inferred that due to the enhanced primary antioxidants in C. ciliaris the reduction in the biomass was comparatively lesser than P. maximum and, hence, classified P. maximum as more sensitive to EO3. In another study, Dolker and Agrawal [68] subjected two other common grass species of IGP to EO3, namely, Ischaemum rugosum Salisb. and Malvestrum coromandelianum L. which belonged to C3 and C4 categories, respectively, at two different growth stages. They concluded that M. coromandelianum was more responsive to the applied stress regarding growth and total biomass than I. rugosum. Furthermore, it was established that I. rugosum maintained both growth and development by partitioning the resources efficiently under EO3 stress (Fig. 3).

The grassland community makes a remarkable contribution to biodiversity on a global scale; hence, prioritizing the evaluation of the components (both structural and functional) of seminatural grassland communities to surface O3 is equally important as crops [69,70,71]. Dolker et al. [72] also studied the response of tropical grassland species to EO3 stress at the community level in a semi-natural grassland. They observed that all the species significantly reduced their above and belowground biomass under EO3 compared to the ambient conditions. A reduction in the root shoot ratio of the species indicated a lower allocation of carbon to the root system, which will ultimately hamper the carbon sequestration of the grassland under EO3. Another recent study by Dolker et al. [73] compared the performance of EO3 to ambient O3 treatment in terms of community production, distribution of biomass (grass/forb) at different canopy layers, and the influence of EO3 treatment on the intact community over the exposure period of three years. It was observed that O3 alters the structural and functional properties of a grassland at the community level as different constituent species possess variable sensitivity to it [71]. The community in early successional stage has observed reductions in species richness (SR), evenness (E) and Shannon index (H') upon exposure to EO3 [74]. The study also established that increased colonization of O3-tolerant species has resulted in a decline in species evenness. Among the studied species, the EO3 treatment had a greater detrimental effect on legumes such T. resupinatum, M. officinalis, and D. triflorum in comparison to grasses. It was also inferred that O3 could modify the competitive relationship or plant-plant interaction, which would impact the structural and functional integrity of the community. In the study, community level productivity of the above ground biomass and total biomass decreased, the latter showing a greater drop. It indicated that EO3 has more deterioration at below ground level.

3.6 Model-driven studies

In an effort to gain a better knowledge of O3 impacts on vegetation, a new generation of dynamic process-based models is being developed and implemented. Using world scale modelling, Van Dingenen et al. [75] evaluated the effects of tropospheric O3 on crops and estimated that yearly yield losses for rice and wheat in India would be between 6 and 8% and 13 to 28%, respectively. According to Ghude et al. [76], the Weather Research and Forecasting model in conjunction with the Chemistry (WRF Chem) model indicated losses of 2.1 ± 0.8% for rice and 3.5 ± 0.8% for wheat, with the greatest losses happening in central and northern India. Following a reanalysis of yield loss in India using the WRF-Chem model, Sharma et al. [77] discovered yield losses in rice and wheat of 21% and 6%, respectively, which are significantly larger than yield losses in earlier research. A study conducted on four Indian wheat cultivars over a two-year period was analyzed using an O3- flux model showed that, under ambient conditions with + 20 ppb O3, the loss in grain yield was greater in early seeded cultivars (23.9% ± 1.35) than in late sown cultivars (11.5% ± 0.37) [33].

4 Mechanism of response and trade-off strategies in ozone-exposed plants

In this section, we attempt to consolidate the mechanism of cellular responses (Fig. 4) and trade-off strategies of the plants under O3 stress, which might have led to an alteration in the yield and productivity of the exposed plants. Stomata are crucial in determining the O3 flux into the apoplastic region of plants since the major uptake of O3 occurs through the stomata present on the leaf surface. The stomatal flux depends on various resistances at physiological and morphological levels- aerodynamic resistance, boundary resistance, stomatal resistance, and internal resistance in the leaves after stomatal uptake of O3 [78]. Stomatal regulation is one of the key determinants of O3 sensitivity in plants. Since the stomatal aperture often decreases upon exposure to O3, plants that rapidly regulate their stomatal aperture are categorized as resistant/ tolerant. This restriction of the O3 entry serves as the first line of cellular defense against the damage caused by O3. The studies on wheat reflected the higher stomatal conductance to be the main culprit behind the reduction in yield together with the photosynthate trade-off to defence rather than reproduction [33,34,35, 38, 53]. The reduced stomatal conductance affects the plants' carbon fixation ability, which severely hampers the related metabolic pathways and thereby considerably reduces the yield [39, 40, 64]. In the case of maize, the stomatal conductance was responsible for the reduction in photosynthesis and yield [45, 46]. Few studies have also reported anatomical adaptations in the plants to reduce the uptake of O3, such as reducing the leaf area index, stomatal density, and increased trichome density [35, 48, 51, 62] which will further restrict the stomatal conductance of O3 and will better adapt the plants to the exposed stress. Studies focusing on the responses of leguminous crops have reported prolonged stomatal closure under O3 stress, which also impairs the carbon fixation ability and yield [41].

Fig. 4
figure 4

(Modified from Sarkar et al. [79])

Detailed mechanism of O3 uptake and cellular response in plants. AA ascorbic acid, APX ascorbate peroxidase, AA/DHA T ascorbic acid/dehydroascorbate transporter, CAT catalase, Cytb561 Cytochrome b, DHA dehydroascorbate, DHAR dehydroascorbate reductase, GR glutathione reductase, H2O2 hydrogen peroxide, H2O water, MDA monodehydroascorbate radical, MDAR monodehydroascorbate reductase, NA + -AA T Na-dependent L-ascorbic acid transporter, O2.− superoxide radical, O2, oxygen, POD peroxidase, ROS reactive oxygen species, SOD superoxide dismutase.

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After entering the cell in the apoplastic region, O3 has two possible fates: it can either directly act on the plasma membrane through a process of ozonolysis or initiate the excess production of ROS in the apoplastic region (Fig. 4). It has been observed that the O3 sensitive plants undergo higher oxidative stress which is counterbalanced by enhancing the array of antioxidants (enzymatic and non-enzymatic) and hence they suffered greater loss of yield and productivity. The higher upregulation of antioxidants was reported in the tolerant plants, while sensitive ones failed to balance the increased ROS produced due to O3 exposure. There is a differential regulation of antioxidants depending upon the site of oxidative stress. Some studies have reported an increase in the ascorbic acid content, which signifies a direct reaction of O3 with the apoplastic ascorbate, in turn reducing the membrane damage in the resistant plants [41,42,43, 52,53,54]. The induced oxidative stress further leads to the peroxidation of the lipid content of the cell membrane. It damages the photosynthetic pigments and can trigger multiple signaling cascades. The ROS can enter intracellular spaces directly or through specific protein channels and trigger the exchange of antioxidants between symplast and apoplast [80]. Within the cell, GSH and ascorbate regeneration were closely correlated, and transport activity was stimulated to refill the depleted ascorbate pool in the apoplast [81]. Several enzymatic antioxidants work together to degrade O2− and H2O2 effectively. Catalase and peroxidase play a role in the conversion of H2O2 to H2O. Glutathione also participates in this protective function [82]. Studies have reported an increase in the enzymatic antioxidants and a trade-off between defence and reproduction under O3 stress and defence and growth [59, 61].

The studies dealing with the response of perennial plants showed increased enzymatic antioxidants, which induced better tolerance to the plant at later growth stages [63]. Among the studied agricultural crops, the study on rice by Ramya et al. [32] inferred the yield reduction due to O3 result from a trade-off between the photoassimilate allocation to defence rather than reproduction. Another trade-off between growth and reproduction was observed in perennial plants by Singh et al. [65], establishing height-diameter allometry in M. indica, which imparts higher tolerance in the plant under O3 stress.

5 Conclusion

Ozone pollution has drastically increased in the past few years, and it is predicted to worsen in the coming years due to its widespread sources despite the changes in policies and pollution control norms. There is a need to strengthen the O3 monitoring network in the Indian subcontinent, particularly in the rural areas, to provide realistic monitoring data for effective use in prediction modeling. The reviewed literature clearly indicates significant adverse impacts of elevated O3 on the Indian vegetation including crops, grassland and trees. The sensitivity of the plants to O3 differs depending on the cultivars, phenology, and the species-specificity to the stress. Wheat is the most sensitive crop while maize is the least sensitive one. Rice and leguminous crops are intermediately sensitive. Among the horticultural crops, leafy vegetable, Beta vulgaris is most sensitive, Solanum tuberosum and Solanum lycopersicum are intermediate and Abelmoschus spp. is the least sensitive to elevated O3 stress. The important active ingredients of the medicinal plants (Costus pictus < Cymbopogon flexuosus < Sida cordifolia) are mostly increased whereas the biomass decreased under EO3, suggesting their cultivation in the areas with high O3 concentration to exploit the pharmaceutically important compounds. Among the grasses at community level, forbs were found to be highly sensitive to elevated O3 than grasses. Under O3 stress, plants reduce their stomatal flux as an adaptive response resulting in restricted O3 uptake which also compromise the photosynthetic performance of the plants. It turns out that plants under O3 stress have to maintain other demands under reduced photoassimilate formation and hence they adopt various trade-off strategies. The response pattern of various plants studies established that the plants that manipulated their stomatal conductance along with diverting their trade-off strategies were most tolerant to O3 compared to those that only modified the trade-off strategies. The study has also reflected decrease in the nutritional quality of the crops, which will further contribute to the hidden hunger. Hence, there is a prodigious need to ensure food security by focusing on the development of O3-resilient crops to fulfill the demand of the increasing population, along with implementing the stringent policies to reduce O3 pollution.

6 Future prospects

The studies focusing on the impact of O3 on tropical tree species are very less and hence, there is a need to increase the related experiments as trees are a part of major vegetation cover in India. Other prevalent stresses in the tropics include high temperature, other air pollutants (particulate matter, CO2, etc.), drought, and salinity, which further contribute to O3-induced responses (synergistically or antagonistically). Hence, there is a need to have more interactive studies that can screen the better performing plants and their varieties. In India, network programs are required to evaluate the yield and productivity losses across the nation. In order to identify the air quality and climatic conditions, O3 biomonitoring and assessment programs utilizing the common O3 sensitive biomonitors should be promoted. Some biomonitoring concepts, like the NASA Ozone Bioindicator Garden project and the Ozone Gardens of ICP Vegetation, have recently been introduced to create gardens with ozone resistant and sensitive plant varieties. Such concepts need to be immediately implemented in India with increasing public awareness for the threats that tropospheric O3 poses in the region. The accessibility to cost-effective remediation methods should be encouraged in the rural and sub-urban areas.