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

Abstract

The processes involved in cadmium detoxification in plants deeply affect sulfate uptake and thiol homeostasis and generate increases in the plant nutritional request for sulfur. Here, we present an analysis of the dependence of Arabidopsis growth on the concentration of sulfate in the growing medium with the aim of providing evidence on how plants optimize growth at a given sulfate availability. Results revealed that short-term (72 h) exposure to a broad range of Cd concentrations (0.1, 1, and 10 μM) inhibited plant growth but did not produce any significant effects on the growth pattern of both shoots and roots in relation to the external sulfate. Conversely, long-term (22 days) exposure to 0.1 μM Cd significantly changed the pattern of fresh weight accumulation of the shoots in relation to the external sulfate, without affecting that of the roots, although their growth was severely inhibited by Cd. Moreover, under long-term exposure to Cd, increasing the sulfate external concentration up to the critical value progressively reduced the inhibitory effects exerted by Cd on shoot growth, indicating the existence of sulfate-dependent adaptive responses protecting the shoot tissues against Cd injury. Transcriptional induction of the high-affinity sulfate transporter genes (SULTR1; 1 and SULTR1; 2) involved in sulfate uptake by roots was a common adaptive response to both short- and long-term exposure to Cd. Such a response was closely related to the total amount of non-protein thiols accumulated by a single plant under short-term exposure to Cd, but did not showed any clear relation with thiols under long-term exposure to Cd. In this last condition, Cd exposure did not change the level of non-protein thiols per plant and thus did not alter the nutritional need for sulfur. In conclusion, our results indicate that long term-exposure to Cd, although it induces sulfate uptake, decreases the capacity of the Arabidopsis roots to efficiently absorb the sulfate ions available in the growing medium making the adaptive response of SULTR1; 1 and SULTR1; 2 “per se” not enough to optimize the growth at sulfate external concentrations lower than the critical value.

Knock-Down of the Phosphoserine Phosphatase Gene Effects Rather N- Than S-Metabolism in Arabidopsis thaliana

“…Apparently, roots – as the first target of Cd exposure – are of central significance for compensating the negative effects of Cd by detoxification via sulfur metabolism. Detoxification is thought to be mediated by an increased amount of total NPT and phytochelatins (PCs) in roots chelating the Cd taken up (Nocito et al, 2006; Sun et al, 2007; Jozefczak et al, 2014; Ferri et al, 2017). Thus, enhanced SO 4 2- reduction and assimilation in the leaves in response to Cd will only be required, if Cd uptake exceeds the detoxification capacity of the roots and, as a consequence, Cd is transported to the leaves.…”

Glutathione and Its Biosynthetic Intermediates Alleviate Cesium Stress in Arabidopsis

“…Expression of genes encoding high-affinity sulphate transporters in roots, SULTR1;1 and SUTLR1;2, is known to be induced by sulphate starvation (Takahashi et al, 2000;Yoshimoto et al, 2002). These transcripts have also been shown to be increased in response to cadmium and sodium stress (Cao et al, 2014;Yamaguchi et al, 2016;Ferri et al, 2017). However, SULTR1;1 and SULTR1;2 were not induced in response to cesium stress but SULTR1;2 was rather reduced by cesium treatment in the presence of sulphur supply in the optimal potassium condition (Figure 3).…”

“…The b-tubulin gene (TUB2, At5g62690) was used as a reference gene. The primer sequences for HAK5, VSP2, PDF1.2, SULTR1;1, SULTR1;2, SULTR3;1, SULTR3;2, SULTR3;3, SULTR3;4, and SULTR3;5 are shown in the previous publications (Adams et al, 2013;Cao et al, 2014;Ferri et al, 2017). The rest of the primers used are listed in Supplementary Table S1.…”

“…Some examples of the interaction between metal stress and the sulphur metabolic pathway in plants are introduced here. Cadmium exposure in Arabidopsis induces expression of genes encoding sulphate transporter (SULTR), serine acetyltransferase (SERAT), g-glutamylcysteine (g-Glu-Cys) synthetase (GSH1), and GSH synthetase (GSH2) and in turn increases sulphate uptake and accumulation of cysteine (Cys) and PCs (Xiang and Oliver, 1998;Howarth et al, 2003;Yamaguchi et al, 2016;Ferri et al, 2017). Chromium has been shown to induce PC synthase genes (PCS1 and PCS2) and increase hydrogen sulfide, Cys and GSH levels, while copper induces GSH1 and GSH2 in Arabidopsis (Xiang and Oliver, 1998;Fang et al, 2016).…”

Sulphur and biothiol metabolism determines toxicity responses and fate of mercury in Arabidopsis

“…Sulphate uptake is a bottleneck in plant sulphur incorporation, which were upregulated under metal stress, such as SULTR1;1 in roots of maize (Nocito et al, 2006) and Arabidopsis (Ferri et al, 2017). However, other members of the SULTR transporter gene family in Chinese cabbage plantlets and sorghum responded in different manner in leaves and roots under metal stresses (Shahbaz et al, 2014;Akbudak, Filiz, & Kontbay, 2018).…”