Amelioration of the Oxidative Stress Generated by Simple or Combined Abiotic Stress through the K⁺ and Ca2+ Supplementation in Tomato Plants

Abstract

Abiotic stressors such as drought, heat, or salinity are major causes of yield loss worldwide due to the oxidative burst generated under these conditions. Recent studies have revealed that plant response to a combination of different environmental stressors is unique and cannot be deduced from the response developed to each stress when applied individually. Some studies have demonstrated that a different management of some nutrients in the irrigation solution may provide an advantage to the plants against abiotic stressors. Thus, the aim of this study was to investigate if an increase in potassium (K⁺) and calcium (Ca²⁺) concentration in the nutrient solution may have a positive effect on the amelioration of oxidative stress which occurs under the combination of salinity and heat in tomato plants. Our results indicated that plants irrigated with an increase in K⁺ and Ca²⁺ concentrations in the irrigation solution from 7mM (K⁺) to 9.8 mM and from 4 mM (Ca²⁺) to 5.6 mM, respectively, induced a recovery of the biomass production compared to the plants treated with salinity or salinity + heat, and subsequently irrigated with the regular Hoagland solution. This was correlated with a better performance of all the photosynthetic parameters, a reduction in the foliar concentration of H₂O₂ and a lower lipid peroxidation rate, and with a better performance of the antioxidant enzymes ascorbate peroxidase ascorbate peroxidase (APX), dehydroascorbate reductactase (DHAR), glutathione reductase (GR), and NADPH oxidase. Our results showed that these enzymes were differentially regulated at the transcriptional level, showing a higher reactive oxygen species (ROS) detoxification efficiency under salinity and under the combination of salinity and heat, as compared to those plants irrigated with common Hoagland. An increase in K⁺ and Ca²⁺ in the irrigation solution also induced a lower Na⁺ accumulation in leaves and a higher K⁺/Na⁺ ratio. Thus, our study highlights the importance of the right management of the plant nutritional status and fertilization in order to counteract the deleterious effects of abiotic stress in plants.

Keywords: ROS detoxification; abiotic stress combination; antioxidant enzymes.; antioxidant-related genes; heat stress; lipid peroxidation; photosynthesis; salinity.

Figure 1

Fresh (A) and dry weight (B) of tomato plants grown under control, salinity (60 mM NaCl) or salinity and higher concentration of K⁺ and Ca²⁺ in the irrigation solution at optimal temperature (25 °C) or heat stress (35 °C). Data represent means ± SE (n = 6). Bars with different letters within each panel represent data with significant differences at p < 0.05 (Turkey HSD).

Figure 2

Ca²⁺, K⁺ and Na⁺ concentration (A–C) and K⁺/Na⁺ ratio (D) in tomato leaves grown under control, salinity (60 mM NaCl) or salinity combined with higher K⁺ and Ca²⁺ concentration in the irrigation solution under optimal temperature (25 °C) or under heat stress (35 °C). Values represent means ± SE (n = 6). Bars with different letters represent data with significant differences at p < 0.05 (Tukey HSD).

Figure 3

Photosynthetic parameters in tomato leaves grown under control, salinity (60 mM NaCl or salinity combined with higher K⁺ and Ca²⁺ concentration in the irrigation solution at optimal temperature (25 °C) or heat stress (35 °C). Values are means ± SE (n = 6). Bars with different letters within each panel represent data with significant differences at p < 0.05 (Tukey HSD).

Figure 4

H₂O₂ concentration (A) and Lipid peroxidation rate, measured as MDA concentration (B) in tomato leaves grown under control, salinity (60 mM NaCl) or salinity combined with a higher concentration of K⁺ and Ca²⁺ in the irrigation solution at optimal temperature (25 °C) or under heat stress (35 °C). Values represent means ± SE (n = 6). Bars with different letters within eahc panel represent data with significant differences at p < 0.05 (Tuket HSD).

Figure 5

Oxidative metabolism-related gene expression (A) and enzymatic activities (B) in tomato leaves grown under control, salinity (60 mM NaCl) or salinity and higher concentration of K⁺ and Ca⁺² in the irrigation solution at optimal temperature (25 °C) or heat stress (35 °C). Red color represents a higher relative expression or activity with respect to control plants and blue color represents a lower relative expression or activity. Scale is the log₂ values of the expression after normalization with respect to control plants. Absolute values (gene expression and enzymatic activities) as well as log2 values can be found in Supporting Information Tables S2–S5, respectively. Asterisks are representative of significant differences with respect to control plants (p < 0.05).