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Plant Sulfur Metabolism — the Reduction of Sulfate to Sulfite Julie Ann Bick and Thomas Leustek∗

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Plant Sulfur Metabolism — the Reduction of Sulfate to Sulfite Julie Ann Bick and Thomas Leustek∗ 240 Plant sulfur metabolism Ð the reduction of sulfate to sul®te Julie Ann Bick and Thomas Leustek∗ Until recently the pathway by which plants reduce activated matter of contention and is the focus of this review. sulfate to sul®te was unresolved. Recent ®ndings on two Skipping this step for the moment, the remaining reactions enzymes termed 5′-adenylylsulfate (APS) sulfotransferase and in the pathway to cysteine include the reduction of APS reductase have provided new information on this topic. sul®te to sul®de catalyzed by ferredoxin-dependent sul®te On the basis of their similarities it is now proposed that these reductase [6], then assimilation of inorganic sul®de by proteins are the same enzyme. These discoveries con®rm that the sulfhydration of O-acetylserine [7••]. The second the sulfate assimilation pathway in plants differs from that in assimilation pathway branching from APS is used for the other sulfate assimilating organisms. synthesis of a variety of sulfated compounds carried out by speci®c sulfotransferases (ST's). These enzymes use the phosphorylated derivative of APS, 3-phosphoadenosine- Addresses 5′-phosphosulfate (PAPS)[4••,5••], formed by APS kinase Biotechnology Center for Agriculture and the Environment, Rutgers University, 59 Dudley Road, Foran Hall, New Brunswick, New Jersey (AK). 08901-8520 USA ∗e-mail: [email protected] This paper focuses on the latest information on the Current Opinion in Plant Biology 1998, 1:240±244 enzyme catalyzing the reduction of APS. The recent puri®cation of APSSTase from a marine alga provides the http://biomednet.com/elecref/1369526600100240 ®rst evidence on the catalytic properties of this enzyme. At Current Biology Ltd ISSN 1369-5266 the same time, cDNAs have been cloned from the higher Abbreviations plant Arabidopsis thaliana that encode an enzyme termed AK 5′-adenylyl sulfate kinase APS reductase that shows similarities to APSSTase. We APR 5′-adenylylsulfate reductase propose that they are the same enzyme and discuss their APS 5′-adenylylsulfate properties in relationship to a role in sulfate assimilation. APSSTase 5′-adenylylsulfate sulfotransferase PAPS 3′-phosphoadenosine-5′-phosphosulfate Figure 1 Introduction NADP+ This article focuses on a single aspect of a broad subject NADPH H+ area. It is prompted by the recent ®ndings concerning one of the primary steps in the sulfate assimilation GR O-acetylserine GSSG 2– pathway of higher plants. Readers who are interested in GSH 2– Cysteine SO3 S a comprehensive treatment of plant sulfur metabolism are • • APR SiR OASTL referred to several recent reviews [1 ±3 ]. 2– (APSSTase) SO4 APS Higher plants are dependent on inorganic sulfate to ful®l AS their nutritional sulfur requirement. Sulfate is a major AK PAPS Sulfated compounds anionic solute and is required for the synthesis of many ST's different metabolites and coenzymes. After uptake from Current Opinion in Plant Biology the soil, sulfate is either accumulated and stored in the vacuole or it is incorporated into organic compounds The sulfate assimilation pathway in plants. Sulfate is activated by in a process referred to as assimilation. Sulfur can be ATP sulfurylase (AS) forming 5′-adenylylsulfate (APS). APS is a assimilated in one of two ways Ð it is either incorporated branch point intermediate that is used for the reduction pathway •• •• leading to formation of cysteine (upper pathway) or the sulfation as sulfate in a reaction termed sulfation [4 ,5 ], or it is pathway leading to synthesis of various sulfated compounds (lower ®rst reduced to sul®de, the substrate for cysteine synthesis. pathway). The sulfation pathway begins by phosphorylation of APS In plants the majority of sulfur is assimilated in the to 3′-phosphoadenosine-5′phosphosulfate (PAPS) by APS kinase reduced form. (AK). PAPS is the substrate for a variety of sulfotransferases (ST's). In the cysteine pathway, the ®rst reduction step is the topic of this article. We argue that the enzyme APS reductase (APR) is identical The plant sulfate assimilation pathways are depicted to APS sulfotransferase (APSSTase), a glutathione-dependent in Figure 1. The prerequisite step for all metabolic reductase. Its activity is driven by reduced glutathione (GSH) which fates of sulfate is its activation by linkage to 5′-AMP, is recycled from oxidised glutathione (GSSG) through the action forming 5′-adenylylsulfate (APS), a reaction catalyzed of NADPH-dependent glutathione reductase (GR). The subsequent by ATP sulfurylase. APS lies at a metabolic branch reactions are the reduction of sul®te to sul®de by sul®te reductase (SiR) and assimilation of sul®de into cysteine by O-acetylserine (thiol) point Ð it is used either for sulfation or for the reduction lyase (OASTL). pathway. It is the ®rst reduction step that has been a Plant sulfur metabolism Ð the reduction of sulfate to sul®te Bick and Leustek 241 Sulfate reduction in plants analogs) stabilize the enzyme against these inactivating The long-held dogma concerning sulfate reduction stated treatments. that, in plants, APS is the substrate for this reaction and the enzyme APS sulfotransferase (APSSTase) [8]. Although the reaction mechanism of APSSTase has not For a number of reasons, however, the APS pathway been addressed, this is a central issue that should be in plants was not universally accepted [9] Ð despite explored with the puri®ed enzyme. As already mentioned years of research, de®nitive evidence for the existence APSSTase was proposed to be a sulfotransferase. For of APSSTase was not forthcoming. One report of its example, with glutathione as the acceptor S-sulfoglu- puri®cation from Euglena gracilis was confounded by the tathione is formed. It was acknowledged, however, that unreasonably low speci®c activity of the pure enzyme this hypothesis is formed on the basis of inconclusive [10]. Subsequently, another group reported that, in vitro, data and that it is equally plausible that the enzyme is plant APS kinase displays APS sulfotransferase activity a reductase that forms free sul®te [8]. Due to its high as a side reaction [11]. This result, combined with reactivity sul®te can readily form a thiosulfonate with several physical similarities, prompted the idea that reduced thiols [23], possibly explaining the presence of perhaps APS sulfotransferase is a kinetic artefact [11]. thiosulfonate in APSSTase reactions. In contrast to this uncertainty, it is widely believed that prokaryotes (including cyanobacteria) and fungi use PAPS The puri®cation of APSSTase from a macroalga is the for sulfate reduction via the enzyme PAPS reductase ®rst direct and convincing evidence for an APS-dependent [12,13]. Recently, however, direct evidence was published reduction pathway in plants. Additional and complemen- by three independent groups. con®rming the existence of tary evidence for such a pathway was contemporaneously an APS-dependent pathway in plants [14••±16••]. obtained using molecular genetic methods as described in the next section. APS sulfotransferase The APR cDNAs encoding APS reductase Although APSSTase has long been the focus of inves- APS reductase (APR) was identi®ed serendipitously by searching for cDNAs encoding plant PAPS reductase tigation [17] its puri®cation to homogeneity proved to •• •• be an elusive goal. Kanno et al. [14••] ®nally succeeded [15 ,16 ]. Three different cDNAs were cloned from in isolating the enzyme from a marine macroalga by Arabidopsis thaliana (APR1, 2 and 3) that are able to maintaining high levels of ammonium sulfate throughout complement the cysteine auxotrophy of an Escherichia coli the puri®cation procedure. Previous publications noted the cysH (PAPS reductase) mutant strain. The APR cDNAs lability of APSSTase and that it could be stabilized with encode individual members of a small, highly conserved high concentrations of sulfate salts [18], but this ®nding gene family. was never incorporated into a puri®cation scheme. Analysis of the APR isoenzymes revealed that, unlike PAPS reductase, they use APS preferentially over PAPS. As re¯ected by its name, APSSTase was proposed to This property was demonstrated both by in vitro assays catalyze the transfer of sulfate from APS to a thiol acceptor and by in vivo functional complementation of a cysC molecule forming a thiosulfonate [8]. In vitro, many dif- (APS kinase) mutant of E. coli with the APR cDNAS. ferent reduced thiol compounds, including dithiothreitol, An APS reductase would be expected to bypass both can serve as the acceptor. The physiological acceptor was the cysC and cysH mutations in E. coli. Another key envisaged to be glutathione, primarily because it is an difference is that, while PAPS reductase is dependent ef®cient substrate and is the most abundant thiol in the on the redox proteins thioredoxin or glutaredoxin as a chloroplast stroma in which APSSTase is localized [19]. source of electrons, the activity of the APR enzymes is not The algal enzyme shows a kinetic constant for glutathione stimulated in vitro by the addition of E. coli or Spirullina sp. of 0.6 mM, a value that is well below the physiological thioredoxin. Also, the APR cDNAs are able to complement concentration in the stroma, reported to be between 3 and a thioredoxin/glutaredoxin double mutant of E. coli. 10 mM [20,21]. This is a key ®nding that supports much of the earlier work on this enzyme. For example, it has long The properties of the APR enzymes are remarkably similar been known that sul®te production from sulfate is not light to those of APSSTase with respect to optimum assay dependent, requiring only ATP and glutathione (it is not conditions, kinetic constants and inhibitors. A key feature in¯uenced by NADPH or ferredoxin) [22]. is that like APSSTase the APR enzymes are able to use a variety of reduced thiol compounds such as dithiothreitol Puri®ed algal APSSTase has a high catalytic activity and glutathione as a sole source of electrons. The enzyme ±1 ±1 (10.3 µmol min mg protein) and a high af®nity for APS shows a Km for glutathione of 0.6 mM and can only (Km = 2.1 µM).
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