Age-dependent increase in α-tocopherol and phytosterols in maize leaves exposed to elevated ozone pollution

Abstract

Tropospheric ozone is a major air pollutant that significantly damages crop production around the world. Crop metabolic responses to rising chronic ozone stress have not been well-studied in the field, especially in C4 crops. In this study, we investigated the metabolomic profile of leaves from two diverse maize (Zea mays) inbred lines and the hybrid cross during exposure to season-long elevated ozone (~100 nL L−1) in the field using free air concentration enrichment (FACE) to identify key biochemical responses of maize to elevated ozone. Senescence, measured by loss of chlorophyll content, was accelerated in the hybrid line, B73 x Mo17, but not in either inbred line (B73 or Mo17). Untargeted metabolomic profiling further revealed that inbred and hybrid lines of maize differed in metabolic responses to ozone. A significant difference in the metabolite profile of hybrid leaves exposed to elevated ozone occurred as leaves aged, but no age-dependent difference in leaf metabolite profiles between ozone conditions was measured in the inbred lines. Phytosterols and α-tocopherol levels increased in B73 x Mo17 leaves as they aged, and to a significantly greater degree in elevated ozone stress. These metabolites are involved in membrane stabilization and chloroplast reactive oxygen species (ROS) quenching. The hybrid line also showed significant yield loss at elevated ozone, which the inbred lines did not. This suggests that the hybrid maize line was more sensitive to ozone exposure than the inbred lines, and up-regulated metabolic pathways to stabilize membranes and quench ROS in response to chronic ozone stress.

Testing unified theories for ozone response in C4 species

“…In addition, antioxidants in the apoplast, including ascorbate, glutathione, and phenolic compounds, directly scavenge ROS (Ainsworth, 2017; Grace & Logan, 2000; Wedow et al, 2021a). However, previous studies have failed to demonstrate a clear pattern of correlation between O 3 sensitivity and antioxidant compound levels among diverse species (Betzelberger et al, 2010; Choquette et al, 2020; Li et al, 2016; Wedow et al, 2021b). Furthermore, variation in plant responses to O 3 may also be partly explained by genetic background (Choquette et al, 2019; Sorgini et al, 2019).…”

“…This further suggests that C 4 crops may have lower stomatal O 3 uptake than C 3 crops. Nevertheless, previous studies have shown significant impacts of O 3 on maize ( Zea mays ) (Choquette et al, 2019, 2020; Sorgini et al, 2019; Wedow et al, 2021b; Yendrek et al, 2017a, 2017b), switchgrass ( Panicum virgatum ) (Li et al, 2019) and sugarcane (Saccharum spp.) (Moura et al, 2018), but not on sorghum ( Sorghum bicolor L.) (Li et al, 2021) under field conditions, implying the adverse effects of O 3 on plant photosynthesis and productivity vary among C 4 species and genotypes.…”

Approaches to investigate crop responses to ozone pollution: from O3‐FACE to satellite‐enabled modeling

“…So far, only four C 4 crops have been studied for O 3 response using O 3 -FACE facilities (Table 1). Research from SoyFACE showed elevated O 3 concentrations (approximately 100 ppb) significantly reduced leaf photosynthetic capacity in maize (Choquette et al, 2019(Choquette et al, , 2020Sorgini et al, 2019;Wedow et al, 2021b;Yendrek et al, 2017a,b), but had little or no effect on photosynthesis and biomass yield in switchgrass (Li et al, 2019a) and sorghum (Li et al, 2021). These studies also reported considerable genotypic variation in O 3 sensitivity among maize and sorghum lines (Choquette et al, 2019;Li et al, 2021;Yendrek et al, 2017a,b).…”

“…For instance, changes in activity of enzymes involved in ROS metabolism and detoxification (namely catalase [CAT], superoxide dismutase [SOD], and ascorbate peroxidase [APX]) have been found under chronic O 3 exposure in wheat (Feng et al, 2016) and sugarcane (Moura et al, 2018), and these changes were linked to differential photosynthetic and yield sensitivities to O 3 among genotypes. Wedow et al (2021b) investigated differential sensitivity between two inbred maize lines (B73 and Mo17) and the hybrid cross (B73 x Mo17) in relation to the accumulation of defense metabolites in leaf tissue. Senescence was accelerated in the hybrid compared to the inbred lines under elevated [O 3 ] and O 3 -induced reductions in photosynthetic carbon assimilation during grain filling were greater in the hybrid line, leading to significantly greater yield loss.…”

Plant biochemistry influences tropospheric ozone formation, destruction, deposition, and response

“…Additionally, studies must look beyond ascorbate and glutathione as other metabolites detoxify the cell during O 3 stress. Secondary metabolites, including α-tocopherol and phytosterols, increased in field-grown maize exposed to season-long chronic O 3 stress [97]. To ensure accurate modeling and improved breeding for O 3 tolerance, the temporal and spatial antioxidant response needs to be resolved, perhaps independently for each species.…”