Arsenate disrupts ion balance, sulfur and nitric oxide metabolisms in roots and leaves of pea (Pisum sativum L.) plants

Abstract

Arsenic (As) pollution is a significant environmental problem worldwide. Although this metalloid affects plant growth and productivity, it is usually associated with oxidative stress which affects a diverse range of metabolic pathways. However, an additional hazard of As is its presence in edible parts of plants which constitutes a potential animal and human health risk. We exposed 20-d-old pea (Pisum sativum L.) plants, which were used as a model due to their agronomic importance, to 50 μM arsenate (AsV). We then analyzed physiological and biochemical parameters in roots and leaves to determine the principal metabolic characteristics of sulfur, reactive oxygen and nitrogen species (ROS and RNS) metabolisms as well as NADPH-regenerating systems. AsV triggered a significant reduction in growth parameters and an increase in oxidative markers (lipid and protein oxidation) in both roots and leaves. In addition, AsV induced a high level of biosynthesis of enriched sulfur compounds such as phytochelatins (PC2 and PC3) in both roots and leaves, with a concomitant decrease in reduced glutathione (GSH) content. These changes were accompanied by alterations in antioxidative enzymes, the NADPH-regenerating system and nitric oxide (NO) metabolism. In roots, these changes were associated with a significant increase in the amino acids proline, glycine, glutamic acid and γ-aminobutyric acid (GABA) content as well as endopeptidase activity. Analysis of AsV-treated 63-d-old pea plants, which had already developed pods, also showed that As is mainly restricted to roots. Although our results indicate that 50 μM AsV causes a differential metabolic response in roots and leaves, the biochemical adaptation of roots to palliate the negative impact of As is more pronounced. This may enable pea plants to survive by restricting As accumulation in roots and by reducing the level of As in the edible parts of the pea plant (fruits).