Effects of Cadmium Treatment on the Uptake and Translocation of Sulfate inArabidopsis thaliana

Abstract

Cadmium (Cd) is a highly toxic and non-essential element for plants, whereas phytochelatins and glutathione are low-molecular-weight sulfur compounds that function as chelators and play important roles in detoxification. Cadmium exposure is known to induce the expression of sulfur-assimilating enzymes and sulfate uptake by roots. However, the molecular mechanism underlying Cd-induced changes remains largely unknown. Accordingly, we analyzed the effects of Cd treatment on the uptake and translocation of sulfate and accumulation of thiols in Arabidopsis thaliana Both wild type (WT) and null mutant (sel1-10 and sel1-18) plants of the sulfate transporter SULTR1;2 exhibited growth inhibition when treated with CdCl However, the mutant plants exhibited a lower growth rate and lower Cd accumulation. Cadmium treatment also upregulated the transcription of SULTR1;2 and sulfate uptake activity in WT plants, but not in mutant plants. In addition, the sulfate, phytochelatin and total sulfur contents were preferentially accumulated in the shoots of both WT and mutant plants treated with CdCl, and sulfur K-edge XANES spectra suggested that sulfate was the main compound responsible for the increased sulfur content in the shoots of CdCl-treated plants. Our results demonstrate that Cd-induced sulfate uptake depends on SULTR1;2 activity, and that CdCl treatment greatly shifts the distribution of sulfate to shoots, increases the sulfate concentration of xylem sap and upregulates the expression of SULTRs involved in root-to-shoot sulfate transport. Therefore, we conclude that root-to-shoot sulfate transport is stimulated by Cd and suggest that the uptake and translocation of sulfate in CdCl-treated plants are enhanced by demand-driven regulatory networks.

The Sulfate Supply Maximizing Arabidopsis Shoot Growth Is Higher under Long- than Short-Term Exposure to Cadmium

“…In such a context, the need to maintain GSH homeostasis and continuous Cd chelation induces responses allowing plants to increase sulfate uptake by roots and sulfate entry in the reductive assimilation pathway, as well as to modulate sulfate allocation among the different tissues and organs. Such responses are mainly controlled at transcriptional level and involve transcript accumulation of genes that encode sulfate transporters and activities along the pathways of sulfate assimilation and GSH biosynthesis (Lee and Leustek, 1999; Nocito et al, 2002, 2006; Lancilli et al, 2014; Yamaguchi et al, 2016). The pivotal importance of sulfate uptake in the plant adaptation to Cd stress has recently been underlined by the analysis of the Arabidopsis sultr1; 1-sultr1; 2 double mutant – defective in two distinct high-affinity sulfate transporters (SULTR1; 1 and SULTR1; 2) involved in root sulfate uptake from the rhizosphere – which resulted, under limited sulfate supply, in plants being more sensitive to Cd-induced oxidative stress than the wild type (Liu et al, 2016).…”

Plants prioritize phytochelatin synthesis during cadmium exposure even under reduced sulfate uptake caused by the disruption of SULTR1;2

“…When plants were treated with 20 and 40 mM CdCl 2 , the percentages of GSH and cysteine were decreased in both plant lines, although their contents were not decreased. 18 The contents and percentage of PCs were greatly increased under Cd treatment in both WT and sel1-10; in shoots, percentage of PC2 was 42% and 46%, that of PC3 was 20% and 26%, and that of PC4 was 5.5% and 6.6%, respectively, when treated with 20 and 40 mM CdCl 2 . In roots, percentage of PC2 was 20% and 25%, that of PC3 was 35% and 40%, and that of PC4 was 20% and 19%, in both plant lines treated with 20 and 40 mM CdCl2, respectively.…”

“…Using the plant extracts, sulfate contents were determined by ion chromatography, and cysteine, GSH and PCs contents were analyzed by HPLC-fluorescent detection system after labeling of thiol bases by monobromobimane. 18,19 The percentage of sulfate, thiols, and other sulfur containing compounds in total sulfur were calculated on a dry weight basis using the data previously reported. 18 Total sulfur content in sel1-10 was lower than that in the WT for both shoots and roots in all conditions.…”

“…18,19 The percentage of sulfate, thiols, and other sulfur containing compounds in total sulfur were calculated on a dry weight basis using the data previously reported. 18 Total sulfur content in sel1-10 was lower than that in the WT for both shoots and roots in all conditions. Treatment with 20 and 40 mM CdCl 2 increased total sulfur content in the shoots of both WT and sel1-10.…”

“…Sulfate was the major chemical form of sulfur in Cd-treated shoots. 18 This Cd-induced increase of sulfate is due to the increased uptake and the root-to-shoot transport.…”