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.