Hydrogen sulfide - cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots

Abstract

Cadmium (Cd 2+ ) is a common toxic heavy metal ion. We investigated the roles of hydrogen sulfide (H 2 S) and cysteine (Cys) in plant responses to Cd 2+ stress. The expression of H 2 S synthetic genes LCD and DES1 were induced by Cd 2+ within 3 h, and endogenous H 2 S was then rapidly released. H 2 S promoted the expression of Cys synthesis-related genes SAT1 and OASA1, which led to endogenous Cys accumulation. The H 2 S and Cys cycle system was stimulated by Cd 2+ stress, and it maintained high levels in plant cells. H 2 S inhibited the ROS burst by inducing alternative respiration capacity (AP) and antioxidase activity. H 2 S weakened Cd 2+ toxicity by inducing the metallothionein (MTs) genes expression. Cys promoted GSH accumulation and inhibited the ROS burst, and GSH induced the expression of phytochelatin (PCs) genes, counteracting Cd 2+ toxicity. In summary, the H 2 S and Cys cycle system played a key role in plant responses to Cd 2+ stress. The Cd 2+ tolerance was weakened when the cycle system was blocked in lcddes1-1 and oasa1 mutants. This paper is the first to describe the role of the H 2 S and Cys cycle system in Cd 2+ stress and to explore the relevant and specificity mechanisms of H 2 S and Cys in mediating Cd 2+ stress.Cadmium (Cd 2+ ) is a common toxic heavy metal ion in the environment. It greatly affects the growth and development of plants and is harmful to human health through the food chain 1,2 . Because of its carcinogenic properties and its detrimental effects on the growth of organisms, Cd 2+ contamination of agricultural soil has become a critical concern. Preventing reduced growth and accumulation of Cd 2+ in harvested organs of plants growing on Cd 2+ -contaminated soils has become an urgent task as it can contribute to food safety. Thus, it is important to explore plant stress defense mechanisms and to find ways to reduce the Cd 2+ accumulation in grains.As a heavy metal not participating in redox reactions, Cd 2+ can easily dissolve in water and quickly be taken up by plant roots 3,4 . The physiological consequences of Cd 2+ toxicity in plants are chlorosis, stunted growth, and cell death, among others [5][6][7] . At the cellular level, Cd 2+ can alter protein structure and inhibit enzyme activity by binding to sulfhydryl and carbonyl groups and replacing essential co-factors of enzymes [7][8][9] . The overproduction of reactive oxygen species (ROS) is the primary response of plants to Cd 2+ with negative impact on cell function 10 . Further damage can be caused by ROS-independent, secondary mechanisms. Lipid peroxidation is the most deleterious effect caused by Cd 2+ -induced ROS 4 . Malondialdehyde (MDA), one of the decomposition products of lipid peroxidation, can modify active substrates in plant cells, including nucleic acids, proteins and saccharides 11 . To become resistant to Cd 2+ toxicity, plants have developed several strategies, such as inducing the

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

“…This study was carried out on Arabidopsis (Arabidopsis thaliana), including Col-0 wild type and lcd (SALK_082099), des1-1 (SALK_103855), lcddes1-1 (lcd and des1 cross), and oasa1 (SALK_074242c) mutants (Jia et al, 2016). For the overexpressing lines, OE LCD and OE DCDES, the LCD and DCDES fragments were amplified from total cDNA and cloned into the pCAMBIA1300-35S vector with the restriction sites XbaI and KpnI.…”

Comparative Transcriptome Analysis Uncovers Roles of Hydrogen Sulfide for Alleviating Cadmium Toxicity in Tetrahymena Thermophila

“…H 2 S alleviates Cd toxicity in plants. Exogenous H 2 S recovered Cd-induced growth inhibition in Brassica napus, Arabidopsis, and barley [25][26][27]. 70 µM H 2 S largely stimulated proliferation of T. thermophila (Fig.…”

“…It is well known that antioxidant defense system increases organism tolerance against metal-induced toxicity by upregulating the nonenzymatic antioxidants and different antioxidant enzymes. H 2 S increase GSH content and antioxidant enzymes activity in Arabidopsis [26]. Under Cd stress, GSH content increased by 51% and exogenous H 2 S supplement further increased the GSH content in T.…”

Multidirectional Changes in Parameters Related to Sulfur Metabolism in Frog Tissues Exposed to Heavy Metal-Related Stress

“…Their toxicity also affects the levels of sulfane sulfur-containing compounds ( Table 4, Figure S1 Supporting information), which in case of the enhanced ROS generation may show their antioxidative properties [11]. Jia et al [55] suggested that the H 2 S and Cys cycle system is a key regulator of the response to cadmium-stress in plants that acts to induce and maintain levels of bioactive molecules (H 2 S, Cys, GSH and MTs) that improve plant resistance to cadmium-stress. Our results confirmed some of the results by Jia et al [55], namely, that the CTH gene expression up-regulation results in the elevated Cys level in the liver (Tables 4 and 5), Similarly, the MPST gene expression up-regulation results in the elevated Cys and GSH levels (Tables 4 and 5).…”

“…Jia et al [55] suggested that the H 2 S and Cys cycle system is a key regulator of the response to cadmium-stress in plants that acts to induce and maintain levels of bioactive molecules (H 2 S, Cys, GSH and MTs) that improve plant resistance to cadmium-stress. Our results confirmed some of the results by Jia et al [55], namely, that the CTH gene expression up-regulation results in the elevated Cys level in the liver (Tables 4 and 5), Similarly, the MPST gene expression up-regulation results in the elevated Cys and GSH levels (Tables 4 and 5). The present report is the first to widely describe the role of the sulfane sulfur/H 2 S generating enzymes and the Cys/glutathione system in Pb 2+ , Hg 2+ and Cd 2+ stress, in various frog tissues, and to explore the mechanisms mediating heavy metal related stress.…”