The activity of ATP sulfurylase extracted from roots of intact canola (Brassica napus 1. cv Drakkar) increased after withdrawal of the S source from the nutrient solution and declined after refeeding S0,'-to S-starved plants. The rate of S0,'-uptake by the roots was similarly influenced. ldentical responses were obtained in SO,'--fed roots when one-half of the root system was starved for S. S is predominantly available to higher plants as S0,'-taken up from soil by the roots. The rate of S uptake by plant roots, especially those of crop species, which have been bred for their fast growth capacity and high harvest potential, is controlled by regulatory processes that operate in such a way that the needs of the whole organism are matched by rates of S uptake. A good illustration of this behavior is provided by the severalfold enhancement of S0: -uptake observed in plants previously deprived of S for periods of a few hours to a few days (

SummarySulfate uptake and ATP sulfurylase activity in the roots of Arabidopsis thaliana and Brassica napus were enhanced by S deprivation and reduced following resupply of SO 4 2-. Similar responses occurred in split-root experiments where only a portion of the root system was S-deprived, suggesting that the regulation involves inter-organ signaling. Phloem-translocated glutathione (GSH) was identified as the likely transducing molecule responsible for regulating SO 4 2-uptake rate and ATP sulfurylase activity in roots. The regulatory role of GSH was confirmed by the finding that ATP sulfurylase activity was inhibited by supplying Cys except in the presence of buthionine sulfoximine, an inhibitor of GSH synthesis. In direct and remote (split-root) exposures, levels of protein detected by antibodies against the Arabidopsis APS3 ATP sulfurylase increased in the roots of A. thaliana and B. napus during S starvation, decreased after SO 4 2-restoration, and declined after feeding GSH. RNA blot analysis revealed that the transcript level of APS1, which codes for ATP sulfurylase, was reduced by direct and remote GSH treatments. The abundance of AST68 (a gene encoding an SO 4 2-transporter) was similarly affected by altered sulfur status. This report presents the first evidence for the regulation of root genes involved in nutrient acquisition and assimilation by a signal that is translocated from shoot to root.

The dual role of glutathione as a transducer of S status (A.C. Lappartient and B. Touraine [1996]Plant Physiol 11 1 : 147-1 57) and as an antioxidant was examined by comparing the effects of S deprivation, glutathione feeding, and H202 (oxidative stress) on S0,'-uptake and ATP sulfurylase activity in roots of intact canola (Brassica napus L.). ATP sulfurylase activity increased and S0,'-uptake rate severely decreased in roots exposed to 1 0 mM H20,, whereas both increased in S-starved plants. In split-root experiments, an oxidative stress response was induced in roots remote from H20, exposure, as revealed by changes in the reduced glutathione (CSH) leve1 and the CSH/oxidized glutathione (CSSC) ratio, but there was only a small decrease in Soa2-uptake rate and no effect on ATP sulfurylase activity. Feeding plants with GSH increased CSH, but did not affect the CSH/CSSC ratio, and both ATP sulfurylase activity and S0,'-uptake were inhibited. The responses of the H,O,-scavenging enzymes ascorbate peroxidase and glutathione reductase to S starvation, CSH treatment, and H,O, treatment were not to glutathione-mediated S demand regulatory process. W e conclude that the regulation of ATP sulfurylase activity and S0,'-uptake by S demand is related to CSH rather than to the CSH/CSSC ratio, and is distinct from the oxidative stress response.In higher plants the activity of root uptake systems is regulated so that the total intake of a nutrient depends on the plant's need for this element rather than on its concentration in the rooting medium. Experimentally, this behavior is translated into a specific increase of ion uptake rate in plants recovering from hours to days of deficiency of a single element, as has been observed for K+ (De la Guardia et al., 1985; Siddiqi and Glass, 1986,1987), H,PO,-(Clarkson and Scattergood, 1982 Drew and Saker, 1984; Lee, 1993), NO,-(Lee and Rudge, 1986; Bowman et al., 1989; Lee, 1993), and SO2-(Clarkson and Saker, 1989; Hawkesford and Belcher, 1991; Hawkesford et al., 1993; Lee, 1993; Lappartient and Touraine, 1996). This demand-driven regulation of uptake rate is a fundamental feature contributing to the ability of terrestrial plants to maintain nutrient homeostasis in cells of their various tissues and organs despite frequent variations in the root environment. These demand-driven regulatory processes in root activity appear to be controlled by shoots via phloem-translocated signals, as has been described for NO,-uptake (Imsande and Touraine, 1994; Touraine et al., 1994). In the case of SO2-, enhancement of S 0 2 -uptake in a given root was observed when other roots were deprived of S while the root under observation was continuously fed with SO2- (Clarkson et al., 1983; Lappartient and Touraine, 1996). Moreover, in canola (Brassica napus L.) roots, the activity of ATP sulfurylase, the first enzyme in the SO2-assimilation pathway, showed a similar response to the changes in S nutritional status (Lappartient and Touraine, 1996). Both S0,2-uptake and ATP sulfurylase are probably repres...