Introduction
Ozone is a double edged sword, protecting life system from the damage of ultraviolet radiation in stratosphere, but generating adverse effects as the concentration rises at the ground level. Among atmospheric pollutants, ground-level ozone (O3) is considered as one of the most detrimental air pollutants (Fiore et al ., 2012; Li & Blande, 2015; Paoletti et al ., 2014). Since the 21st century, a strong increase of O3occurs with an annual average rate of 0.5-2% in the northern mid-latitudes (Stocker, 2014). By 2050, ground-level O3concentrations may rise 20%-25% globally, with comparable value in India and South Asia by 2020 (Dentener et al ., 2005; van Dingenenet al ., 2009). Excessive O3 is not only unhealthy for humans but also detrimental for plants, because elevated O3 limits growth of plants and affects the yield and quality of crops. It is predicted that the elevated O3will reduce annual yield for some crops about 26% by 2030 (Avneryet al ., 2011). The effect of O3 on wheat (Triticum aestivum ) occurs with 6.4-14.9% of yield loss now and this number would rise to 14.8-23.0% by 2020 (Feng et al ., 2015). The production of rice (Oryza sativa ) and soybean (Glycine max ) are also affected by O3, with a significant yield decrease of 14% for rice (Ainsworth, 2008) and 28-35% for soybeans in 2020 (Wang & Mauzerall, 2004) compared with that grown in charcoal filtered air. The loss of crop yield results in great economic losses. Annual crop losses, for example, are estimated at about $3-5.5 billion in China and about $2-4 billion in the US due to the damage of O3, which will increase in the future (van Dingenen et al ., 2009).
It is well known that wheat, rice and soybean are the most important crops worldwide. Wheat is depended on by more than half of the world population (Li et al ., 2016; Saitanis et al ., 2014; Zhuet al ., 2011). Rice is the staple food for the largest number of people on Earth, with total 984 million tons in 2017 (FAO & UNICEF, 2017). Soybean provides vegetable oil for about one third of the world and is also considered as important protein source in Asian countries (Kinney, 1996; Nishinari et al ., 2014). However, there is a gap existed between growing demand and crop production. For example, although the increase in yield of wheat by 2% annually until 2020 required for the human beings, high O3 levels has been accompanied by a loss of production and reduced nutritional value (Biswas et al ., 2008; Feng et al ., 2008; Singh, Huerta-Espino et al ., 2007; Wilkinson et al ., 2012). Therefore, understanding the mechanism by which crops respond to increasing O3 level is pivotal for meeting the increased food demands as the world faces the rapid urbanization, industrialization and climate change.
Previous studies pointed to the negative effects of O3pollution on crop yield by perturbing the multiple aspects and balance of metabolism in plants (Ainsworth, 2008; Emberson et al ., 2009; Li et al ., 2018). It is thought that stomata of leaves provide a route for O3 to enter cells. O3 causes a range of successive modifications including reduced carbon assimilation and photosynthetic rates, chlorophyll loss, leaf bronzing, development of necrotic spots, senescence and eventually the loss of seed mass and number (Chernikova et al ., 2000; Krupa et al ., 2001; Baieret al ., 2005; Fiscus et al ., 2005; Betzelberger et al ., 2010). For defense, carbon skeletons diverts to towards distinct pathways contribute to the synthesis of various metabolic compounds, such as flavonoids, phenolic compounds and lignin (Cabané et al ., 2004; Kontunen-Soppela et al ., 2007; Castagna & Ranieri, 2009; Dizengremel et al ., 2012). For instance, accumulation of lignin assists plants to grow erect, facilitates their photosynthesis, and provides protection (Graham et al ., 2005).
Previous studies to investigate wheat, rice and soybean in response to O3 only reveal drastic reductions in the major leaf photosynthetic, thiol-redox state and carbon metabolism proteins and induction of defense/stress-related proteins (Agrawal et al ., 2002; Ahsan et al ., 2010; Sarkaret al ., 2010; Galant et al ., 2012). However, comparable assessments of metabolome among the three species have not been examined. O3 stress affects many pathways, such as mitochondrial respiration, the pentose phosphate pathway, the shikimate and phenylpropanoid pathways, and the anaplerotic metabolic pathway (Dizengremel et al ., 2012). Accordingly, the activity of a large number of enzymes in these pathways is also affected by O3. Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisco) activity, for example, showed a significant decrease in the presence of O3(Sun et al ., 2014), while a strong increase in the activity of phosphoenolpyruvate carboxylase (PEPc) also occurs (Landolt et al ., 1997; Fontaine et al ., 1999; Renaut et al ., 2009). This PEPc is thought to participate in anaplerotic CO2 fixation and could also lead subsequently to different pathways for amino acid synthesis (Melzer & O’Leary, 1987). Although these processes and enzymes in these pathways have been extensively studied, the exact and specific metabolites in these pathways remains to be elucidated in the three species under elevated O3. The objectives of this study were: 1) to identify components of metabolic composition in wheat, rice and soybean under elevated O3, 2) to investigate which metabolic pathway was influenced, and their similarities and differences among the three crops.