Protectants to ameliorate ozone-induced damage in crops – A possible solution for sustainable agriculture☆
Introduction
Ozone pollution is a serious concern for human life, forests, food security and agricultural productivity (Feng et al., 2022; Paoletti et al., 2022; Proietti et al., 2021; Sicard, 2021). In Asia, extensive agricultural regions in India and China are severely polluted by O3 (Agathokleous et al., 2018a, Ma et al., 2019; Ziemke et al., 2019). Rising precursors like nitrogen oxides (NOx) originating from combustion processes (industrial activities, engine exhaust and electricity generation) (Bărbulescu et al., 2022), volatile organic compounds (VOCs) resulting from various domestic and industrial activities (e.g. coal combustion, cooking, vehicular exhaust, personal care products and construction materials) (Norris et al., 2022) and carbon monoxide emitted from hydrocarbon oxidation and burning of fossil fuels and biomass (Girach and Nair, 2014), are the primary drivers of O3 pollution. As of 2014, the two major precursors namely NOx and non – methane VOCs (NMVOCs) were emitted by Asian countries; wherein China produces 30 and 19% and India emits 13 and 11% of NOx and NMVOCs respectively (Hoesly et al., 2018). Various studies in India have also indicated that O3 is among the most significant air pollutants in rural and suburban regions (Chand and Lal, 2004; Mukherjee et al., 2021; Yadav et al., 2020). Through model simulations, Lu et al. (2018) observed a substantial seasonal fluctuation in India, with higher values (54.1 ppbv) throughout the summer season. Similarly, Hakim et al. (2019) utilised a multi-model to measure O3 levels across India and reported that it ranged from 37.3 to 56.1 ppb, with maximum values in the north.
The impact of O3 on crop characteristics such as growth, biomass, and biochemistry has been well documented (Dhevagi et al., 2022a, 2022b, 2022c; Ramya et al., 2021a, 2021b). Initially, O3 enters the leaf tissues through stomata and as a consequence, reactive oxygen species (ROS) are formed causing degradation of photosynthetic proteins and chlorophylls, damage of membrane and alterations of metabolic activities (Bray and West, 2005; Sarkar et al., 2015). O3 phytotoxicity is widely proven on the field too, and its deleterious influence on crop performance is a serious concern (Chauhan and Sharma, 2023; Gupta et al., 2022; Sonwani et al., 2022). Especially, O3 has a detrimental impact on crop productivity in Asia (Feng et al., 2021, 2022). Hence, food security in India and China, which are already challenged by overpopulation, climate change, resource overutilization and biodiversity loss, is also threatened by O3 concentrations due to serious yield loss (Feng et al., 2022; Mills et al., 2018; Sampedro et al., 2020; Tai et al., 2014). The estimated decline in cereal crop output due to O3 pollution for the year 2030 is between 10 and 48% for wheat and 5–28% for rice (Tai et al., 2021). Reduced crop output would also reduce India's gross domestic product (GDP) (Gadgil and Gadgil, 2006). Furthermore, it has been predicted that the yearly economic losses due to O3 for soybean, maize, wheat and rice are expected to be roughly 9.8–18.8, 5.0–6.0, 10.4–12.5 and 6.7–10.6 billion US dollars between 2010 and 2080 (Sampedro et al., 2020). In addition, Feng et al. (2022) have reported that China records the highest yield loss in rice (23%), wheat (33%) and maize (9%), with a total crop loss of $ 63 billion US Dollars. Hence, understanding the mechanism of O3 influence on agriculture crops and ROS formation might help to limit worldwide yield losses and promote crop production sustainability. Moreover, developing an efficient plant protectant would aid in ameliorating O3 – induced crop loss.
Various strategies were found efficient in alleviating O3 stress in crops. These include maintaining optimal potassium levels (Dunning et al., 1974), inoculation of plant growth promoting rhizobacteria (Estes et al., 2004), increasing nitrogen supply (Schulte auf’m Erley et al., 2007), applying manure and biofertilizers (Calvo et al., 2009; Singh and Agrawal, 2011), offsetting N2O emissions by adopting no tillage practices (Regina and Alakukku, 2010), shifting the crop calendar (Ghude et al., 2014; Teixeira et al., 2011), treating seeds with gamma radiation (Chaudhary and Agrawal, 2014; Moussa, 2011), altering the N–P–K levels (P. Singh et al., 2015; Singh et al., 2012, 2011, 2009; Singh and Agrawal, 2009), proper weed management (Rai et al., 2016), screening for O3 – tolerant cultivars (Ainsworth, 2017; Dhevagi et al., 2022b; Ramya et al., 2021b) and applying chemical protectants (Chaudhary and Rathore, 2020; Feng et al., 2018; Giovannelli et al., 2019; Gupta et al., 2021; Shang et al., 2022). However, each approach has its own shortcomings. For example, although there are various cultivars, only a handful are tolerant to O3, and many high yielding types are vulnerable to O3 stress, emphasising the urgent need for alternative strategies to protect the plants from O3 induced damage. Among all the aforementioned measures, the most extensively used strategy in relieving O3 stress on crops is the use of chemical protectants. As a result, this review aims to present and analyse the current state and recent advances in the use of protectants against O3-induced crop damage in order to provide a viewpoint for food security in an O3-polluted environment.
A wide range of chemical and natural substances like antioxidants, growth regulators, insecticides, antiozonants, plant hormones, and nutrition management have been identified to provide varying degrees of transient protection from O3 injury to plants (Fig. 1) (Chen et al., 2018; Runeckles and Resh, 1975; Saitanis et al., 2015; Y. Zhang et al., 2018). Several studies have demonstrated the efficacy of these compounds in reducing the impacts of acute O3 exposure (Manning, 2000; Agrawal et al., 2005; Tiwari and Agrawal, 2009; Singh and Agrawal, 2009). Application of protectants provides several benefits over other strategies for mitigating the detrimental effects of O3. Although several studies reviewed relevant literatures, most are solely focused on the synthetic chemical ethylenediurea (EDU), and no study reviews the efficacy of different methods in an integrated way (Agathokleous et al., 2021a; Pazarlar, 2022). Hence, this review is first of its kind to summarise the various protectants employed in alleviating O3 stress and identify future research required through the use of bibliometric analysis.
Section snippets
Bibliometric analysis
A bibliometric analysis was carried out by surveying literatures taking into account three dimensions, namely (i) tropospheric ozone (Z), (ii) crop (W), and (iii) protectants (antioxidant or antiozonant or antitranspirants or plant growth regulators or pesticides or nutrient management or plant hormones) (Π) in order to provide an analysis of various types of protectants alleviating the O3 stress in crops. Fig. 2 depicts an analysis of how these three measures might be revisited using
Protectants alleviating O3 stress on crops
The various protectants studied in alleviating O3 stress in crops are categorised into plant-protecting fungicides, antitranspirants, antioxidants, antiozonants, plant hormones, plant growth regulators, and nutrient management (Saitanis and Agathokleous, 2021).
Hormesis – a tool to sustain food security
Hormesis is a highly universal phenomenon that affects virtually all living organisms (Calabrese and Blain, 2011; Calabrese and Mattson, 2017; Jalal et al., 2021). While the (re)evaluation of the research for hormesis in plants took longer than it did for other organisms, efforts made primarily in the last ten years have revealed accumulated empirical evidence to support the hypothesis that toxic substances can increase crop productivity in low doses (Agathokleous and Calabrese, 2019; Christou
Dearth of knowledge
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The current bibliographic analysis highlights that, amongst various potential protectants, the antiozonant EDU seems to be the most studied. Further studies focusing on screening other cost–effective and easily available alternates has become the current need.
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Given the significant absence of assessments of the dose-response relationship for protectants towards the mitigation of O3 stress, further research should concentrate in integrating various sub–NOAEL (no–observed–adverse–effect–level)
Conclusions
Ozone concentrations are rising in developing countries, endangering crop production sustainability and thus food security. As a result, the quest for safe and alternate protectants is becoming increasingly critical. Hence, the present review evaluates the various natural and chemical protectants used to maintain the yield losses in O3-exposed plants. Results revealed that amongst various protectants, EDU is the widely studied protectant to alleviate ozone stress on crops. However, while many
Funding
This work was supported by the Physical Research Laboratory (PRL), Ahmedabad through its Indian Space Research Organisation (ISRO)-Geosphere Biosphere Programme (GBP) under Atmospheric Trace gases Chemistry Transport Modeling (ATCTM) Scheme.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work would like to thank the Physical Research Laboratory (PRL), Indian Space Research Organisation (ISRO), Ahmadabad for providing funding under Atmospheric Trace gases Chemistry Transport Modeling (ATCTM) Scheme and Tamil Nadu Agricultural University for providing all facilities in conducting this study.
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This is an Invited Review discussed with the Special Content Editor G. Benelli.