Elevated CO2 Can Improve the Tolerance of Avena sativa to Cope with Zirconium Pollution by Enhancing ROS Homeostasis

Abstract

Zirconium (Zr) is one of the toxic metals that are heavily incorporated into the ecosystem due to intensive human activities. Their accumulation in the ecosystem disrupts the food chain, causing undesired alterations. Despite Zr's phytotoxicity, its impact on plant growth and redox status remains unclear, particularly if combined with elevated CO₂ (eCO₂). Therefore, a greenhouse pot experiment was conducted to test the hypothesis that eCO₂ can alleviate the phytotoxic impact of Zr upon oat (Avena sativa) plants by enhancing their growth and redox homeostasis. A complete randomized block experimental design (CRBD) was applied to test our hypothesis. Generally, contamination with Zr strikingly diminished the biomass and photosynthetic efficiency of oat plants. Accordingly, contamination with Zr triggered remarkable oxidative damage in oat plants, with concomitant alteration in the antioxidant defense system of oat plants. Contrarily, elevated levels of CO₂ (eCO₂) significantly mitigated the adverse effect of Zr upon both fresh and dry weights as well as the photosynthesis of oat plants. The improved photosynthesis consequently quenched the oxidative damage caused by Zr by reducing the levels of both H₂O₂ and MDA. Moreover, eCO₂ augmented the total antioxidant capacity with the concomitant accumulation of molecular antioxidants (e.g., polyphenols, flavonoids). In addition, eCO₂ not only improved the activities of antioxidant enzymes such as peroxidase (POX), superoxide dismutase (SOD) and catalase (CAT) but also boosted the ASC/GSH metabolic pool that plays a pivotal role in regulating redox homeostasis in plant cells. In this regard, our research offers a novel perspective by delving into the previously unexplored realm of the alleviative effects of eCO₂. It sheds light on how eCO₂ distinctively mitigates oxidative stress induced by Zr, achieving this by orchestrating adjustments to the redox balance within oat plants.

Keywords: Avena sativa; antioxidants; ascorbate/glutathione cycle; oxidative damage; toxic metals.

Figure 1

The combined effect of both eCO₂ and/or Zr upon (A) Zr accumulation, (B) fresh weight and (C) dry weight of oat plants. Four biological replicates were used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.

Figure 2

The combined effect of eCO₂ and/or Zr upon photosynthetic efficiency of oat plants. (A) rate of photosynthesis, (B) chlorophyll fluorescence, (C) stomatal conductance, (D) RuBisco activity, (E) chlorophyll a, (F) chlorophyll b, (G) total chlorophyll, and (H) carotenoids. Four biological replicates were used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.

Figure 3

The combined effect of eCO₂ and/or Zr on the levels of oxidative stress markers of oat plants. (A) hydrogen peroxide (H2O2) and (B) malondialdehyde (MDA). Four biological replicates are used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.

Figure 4

The combined effect of eCO₂ and/or Zr upon the levels of total antioxidant capacity and molecular antioxidants of oat plants. (A) total antioxidant capacity (FRAP), (B) polyphenols, (C) flavonoids. Four biological replicates were used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.

Figure 5

The combined effect of eCO₂ and/or Zr upon the activities of antioxidant oat plants. (A) peroxidase, (B) superoxide dismutase, (C) dehydroascorbate reductase, (D) glutathione peroxidase, (E) catalase, (F) ascorbate peroxidase, (G) monodehydroascorbate reductase, and (H) glutathione reductase. Four biological replicates were used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.

Figure 6

The combined effect of eCO₂ and/or Zr upon the ascorbate/glutathione metabolic pool of oat plants. (A) ascorbic acid, (B) total ascorbate, (C) glutathione, (D) total glutathione, (E) dehydroascorbate, (F) ascorbate/dehydroascorbate ratio, (G) glutathione disulfide and (H) glutathione/glutathione disulfide ratio. Four biological replicates were used to investigate the response. The vertical error bars are the standard error (SE). Fisher’s LSD test (p < 0.05, n = 4) was used for pairwise comparison between groups. The different letters indicate significant differences between the means of each group.