Diversity and regulation of ATP sulfurylase in photosynthetic organisms

. 2014 ; 5 () : 597. [epub] 20141105

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid25414712

ATP sulfurylase (ATPS) catalyzes the first committed step in the sulfate assimilation pathway, the activation of sulfate prior to its reduction. ATPS has been studied in only a few model organisms and even in these cases to a much smaller extent than the sulfate reduction and cysteine synthesis enzymes. This is possibly because the latter were considered of greater regulatory importance for sulfate assimilation. Recent evidences (reported in this paper) challenge this view and suggest that ATPS may have a crucial regulatory role in sulfate assimilation, at least in algae. In the ensuing text, we summarize the current knowledge on ATPS, with special attention to the processes that control its activity and gene(s) expression in algae. Special attention is given to algae ATPS proteins. The focus on algae is the consequence of the fact that a comprehensive investigation of ATPS revealed that the algal enzymes, especially those that are most likely involved in the pathway of sulfate reduction to cysteine, possess features that are not present in other organisms. Remarkably, algal ATPS proteins show a great diversity of isoforms and a high content of cysteine residues, whose positions are often conserved. According to the occurrence of cysteine residues, the ATPS of eukaryotic algae is closer to that of marine cyanobacteria of the genera Synechococcus and Prochlorococcus and is more distant from that of freshwater cyanobacteria. These characteristics might have evolved in parallel with the radiation of algae in the oceans and the increase of sulfate concentration in seawater.

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Allen E., Xie Z. X., Gustafson A. M., Carrington J. C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221. 10.1016/j.cell.2005.04.004 PubMed DOI

Balsera M., Uberegui E., Schuermann P., Buchanan B. B. (2014). Evolutionary development of redox regulation in chloroplasts. Antioxid. Redox Signaling. 21, 1327–1355. 10.1089/ars.2013.5817 PubMed DOI

Beynon J. D., Macrae I. J., Huston S. L., Nelson D. C., Segel I. H., Fisher A. J. (2001). Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm PubMed DOI

Bick J. A., Leustek T. (1998). Plant sulfur metabolism - the reduction of sulfate to sulfite. Curr. Opin. Plant Biol. 1, 240–244. 10.1016/S1369-5266(98)80111-8 PubMed DOI

Bicknell R., Cullis P. M., Jarvest R. L., Lowe G. (1982). The stereochemical course of nucleotidyl transfer catalyzed by ATP sulfurylase. J. Biol. Chem. 257, 8922–8927. PubMed

Bochenek M., Etherington G. J., Koprivova A., Mugford S. T., Malin G., Kopriva S. (2013). Transcriptome analysis of the sulfate deficiency response in the marine microalga PubMed DOI

Bradley M. E., Rest J. S., Li W.-H., Schwartz N. B. (2009). Sulfate activation enzymes: phylogeny and association with pyrophosphatase. J. Mol. Evol. 68, 1–13. 10.1007/s00239-008-9181-6 PubMed DOI

Bromke M. A., Hoefgen R., Hesse H. (2013). Phylogenetic aspects of the sulfate assimilation genes from PubMed DOI

Brunold C. (2000). Regulatory interactions between sulfate and nitrate assimilation, in Sulfur Nutrition and Sulfur Assimilation in Higher Plants, eds De Kok L. J., Stulen I., Rennenberg H., Brunold C., Rauser W. E. (Hague: SPB Academic Publishing; ), 6–75.

Brunold C., Schiff J. A. (1976). Studies of sulfate utilization of algae: 15. Enzymes of assimilatory sulfate reduction in euglena and their cellular localization. Plant Physiol. 57, 430–436. 10.1104/pp.57.3.430 PubMed DOI PMC

Brunold C., Suter M. (1984). Regulation of sulfate assimilation by nitrogen nutrition in the duckweed PubMed DOI PMC

Buchanan B. B., Balmer Y. (2005). Redox regulation: a broadening horizon. Annu. Rev. Plant Biol. 56, 187–220. 10.1146/annurev.arplant.56.032604.144246 PubMed DOI

Canfield D. E. (2004). The evolution of the Earth surface sulfur reservoir. Am. J. Sci. 304, 839–861 10.2475/ajs.304.10.839 DOI

Couturier J., Chibani K., Jacquot J.-P., Rouhier N. (2013). Cysteine-based redox regulation and signaling in plants. Front. Plant Sci. 4:105. 10.3389/fpls.2013.00105 PubMed DOI PMC

Cumming M., Leung S., McCallum J., McManus M. T. (2007). Complex formation between recombinant ATP sulfurylase and APS reductase of PubMed DOI

Dixon D. P., Skipsey M., Grundy N. M., Edwards R. (2005). Stress-induced protein S-glutathionylation in PubMed DOI PMC

Farley J. R., Cryns D. F., Yang Y. H., Segel I. H. (1976). Adenosine triphosphate sulfurylase from PubMed

Farley J. R., Nakayama G., Cryns D., Segel I. H. (1978). Adenosine triphosphate sulfurylase from PubMed DOI

Flombaum P., Gallegos J. L., Gordillo R. A., Rincon J., Zabala L. L., Jiao N., et al. (2013). Present and future global distributions of the marine Cyanobacteria PubMed DOI PMC

Giordano M. (2013). Homeostasis: an underestimated focal point of ecology and evolution. Plant Sci. 211, 92–101. 10.1016/j.plantsci.2013.07.008 PubMed DOI

Giordano M., Pezzoni V., Hell R. (2000). Strategies for the allocation of resources under sulfur limitation in the green alga PubMed DOI PMC

Giordano M., Prioretti L. (2014). Sulphur and algae: metabolism, ecology and evolution, in The physiology of Microalgae, eds Borowitzka M. A., Beardall J., Raven J. A. (Dordrecht: Springer; ).

Giordano M., Raven J. A. (2014). Nitrogen and sulfur assimilation in plants and algae. Aquat. Bot. 118, 45–61. 10.1016/j.aquabot.2014.06.012 DOI

Glaeser K., Kanawati B., Kubo T., Schmitt-Kopplin P., Grill E. (2014). Exploring the PubMed DOI

Harjes S., Bayer P., Scheidig A. J. (2005). The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J. Mol. Biol. 347, 623–635. 10.1016/j.jmb.2005.01.005 PubMed DOI

Hatzfeld Y., Lee S., Lee M., Leustek T., Saito K. (2000). Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from PubMed DOI

Herrmann J., Ravilious G. E., McKinney S. E., Westfall C. S., Lee S. G., Baraniecka P., et al. (2014). Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. J. Biol. Chem. 289, 10919–10929. 10.1074/jbc.M113.540401 PubMed DOI PMC

Holmer M., Storkholm P. (2001). Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw. Biol. 46, 431–451 10.1046/j.1365-2427.2001.00687.x DOI

Sonderby I. E., Geu F. F., Halkier B. A. (2010). Biosynthesis of glucosinolates - gene discovery and beyond. Trends Plant Sci. 15, 283–290. 10.1016/j.tplants.2010.02.005 PubMed DOI

Jagadeeswaran G., Li Y.-F., Sunkar R. (2014). Redox signaling mediates the expression of a sulfate-deprivation-inducible microRNA395 in PubMed DOI

Jones-Rhoades M. W., Bartel D. P. (2004). Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787–799. 10.1016/j.molcel.2004.05.027 PubMed DOI

Kawashima C. G., Matthewman C. A., Huang S., Lee B.-R., Yoshimoto N., Koprivova A., et al. (2011). Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in PubMed DOI

Kopriva S., Mugford S. G., Matthewman C., Koprivova A. (2009). Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep. 28, 1769–1780. 10.1007/s00299-009-0793-0 PubMed DOI

Koprivova A., Giovannetti M., Baraniecka P., Lee B.-R., Grondin C., Loudet O., et al. (2013). Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in PubMed DOI PMC

Lalor D. J., Schnyder T., Saridakis V., Pilloff D. E., Dong A., Tang H., et al. (2003). Structural and functional analysis of a truncated form of PubMed DOI

Lappartient A. G., Touraine B. (1996). Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact canola - The role of phloem-translocated glutathione. Plant Physiol. 111, 147–157. PubMed PMC

Lappartient A. G., Touraine B. (1997). Glutathione-mediated regulation of ATP sulfurylase activity, SO4(2-) uptake, and oxidative stress response in intact canola roots. Plant Physiol. 114, 177–183. PubMed PMC

Lappartient A. G., Vidmar J. J., Leustek T., Glass A. D. M., Touraine B. (1999). Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 18, 89–95. 10.1046/j.1365-313X.1999.00416.x PubMed DOI

Leao G. A., Oliveira J. A., Farnese F. S., Gusman G. S., Felipe R. T. A. (2014). Sulfur metabolism: different tolerances of two aquatic macrophytes exposed to arsenic. Ecotoxicol. Environ. Saf. 105, 36–42. 10.1016/j.ecoenv.2014.03.011 PubMed DOI

Lee S., Leustek T. (1998). APS kinase from PubMed DOI

Lee S. M., Leustek T. (1999). The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci. 141, 201–207 10.1016/S0168-9452(98)00231-3 DOI

Leustek T., Murillo M., Cervantes M. (1994). Cloning of a cDNA-encoding ATP sulfurylase from PubMed DOI PMC

Leustek T., Saito K. (1999). Sulfate transport and assimilation in plants. Plant Physiol. 120, 637–643. 10.1104/pp.120.3.637 PubMed DOI PMC

Leyh T. S. (1993). The physical biochemistry and molecular genetics of sulfate activation. Crit. Rev. Biochem. Mol. Biol. 28, 515–542. 10.3109/10409239309085137 PubMed DOI

Leyh T. S., Taylor J. C., Markham G. D. (1988). The sulfate activation locus of PubMed

Lillig C. H., Schiffmann S., Berndt C., Berken A., Tischka R., Schwenn J. D. (2001). Molecular and catalytic properties of PubMed DOI

Lindahl M., Florencio F. J. (2003). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc. Natl. Acad. Sci. U.S.A. 100, 16107–16112. 10.1073/pnas.2534397100 PubMed DOI PMC

Liu C. X., Suo Y., Leyh T. S. (1994). The energetic linkage of GTP hydrolysis and the synthesis of activated sulfate. Biochemistry 33, 7309–7314. 10.1021/bi00189a036 PubMed DOI

Liu T., Chen J. A., Wang W., Simon M., Wu F., Hu W., et al. (2014). A combined proteomic and transcriptomic analysis on sulfur metabolism pathways of PubMed DOI PMC

MacRae I. J., Segel I. H., Fisher A. J. (2001). Crystal structure of ATP sulfurylase from PubMed DOI

MacRae I. J., Segel I. H., Fisher A. J. (2002). Allosteric inhibition via R-state destabilization in ATP sulfurylase from PubMed DOI

Marchand C., Le Marechal P., Meyer Y., Decottignies P. (2006). Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 6, 6528–6537. 10.1002/pmic.200600443 PubMed DOI

Maruyama-Nakashita A., Nakamura Y., Tohge T., Saito K., Takahashi H. (2006). Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18, 3235–3251. 10.1105/tpc.106.046458 PubMed DOI PMC

Montechiaro F., Giordano M. (2010). Compositional homeostasis of the dinoflagellate PubMed DOI

Mougous J. D., Lee D. H., Hubbard S. C., Schelle M. W., Vocadlo D. J., Berger J. M., et al. (2006). Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol. Cell 21, 109–122. 10.1016/j.molcel.2005.10.034 PubMed DOI

Mueller J. W., Shafqat N. (2013). Adenosine-5-phosphosulfate - a multifaceted modulator of bifunctional 3-phospho-adenosine-5-phosphosulfate synthases and related enzymes. FEBS J. 280, 3050–3057. 10.1111/febs.12252 PubMed DOI PMC

Murillo M., Leustek T. (1995). Adenosine-5′-triphosphate-sulfurylase from PubMed DOI

Parey K., Demmer U., Warkentin E., Wynen A., Ermler U., Dahl C. (2013). Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from PubMed DOI PMC

Patron N. J., Durnford D. G., Kopriva S. (2008). Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol. Biol. 8:39. 10.1186/1471-2148-8-39 PubMed DOI PMC

Phartiyal P., Kim W.-S., Cahoon R. E., Jez J. M., Krishnan H. B. (2006). Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch. Biochem. Biophys. 450, 20–29. 10.1016/j.abb.2006.03.033 PubMed DOI

Ratti S., Knoll A. H., Giordano M. (2011). Did sulfate availability facilitate the evolutionary expansion of chlorophyll a plus c phytoplankton in the oceans? Geobiology 9, 301–312. 10.1111/j.1472-4669.2011.00284.x PubMed DOI

Rauen H. M. (1964). Biochemisches Taschenbuch. Berlin; Heidelberg: Springer.

Ravilious G. E., Herrmann J., Lee S. G., Westfall C. S., Jez J. M. (2013). Kinetic mechanism of the dimeric ATP sulfurylase from plants. Biosci. Rep. 33, 585–591. 10.1042/BSR20130073 PubMed DOI PMC

Rosenwasser S., Van Creveld S. G., Schatz D., Malitsky S., Tzfadia O., Aharoni A., et al. (2014). Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc. Natl. Acad. Sci. U.S.A. 111, 2740–2745. 10.1073/pnas.1319773111 PubMed DOI PMC

Rotte C., Leustek T. (2000). Differential subcellular localization and expression of ATP sulfurylase and 5′-adenylylsulfate reductase during ontogenesis of PubMed DOI PMC

Schiff J. A., Hodson R. C. (1973). The metabolism of sulfate. Annu. Rev. Plant Physiol. 24, 381–414 10.1146/annurev.pp.24.060173.002121 DOI

Schwedock J., Long S. R. (1990). ATP sulphurylase activity of the nodP and nodQ gene products of PubMed DOI

Segel I. H. (1976). Biochemical Calculations: How to Solve Mathematical Problems in General Biochemistry. New York, NY: John Wiley & Sons Inc.

Seubert P. A., Hoang L., Renosto F., Segel I. H. (1983). ATP sulfurylase from PubMed DOI

Seubert P. A., Renosto F., Knudson P., Segel I. H. (1985). Adenosinetriphosphate sulfurylase from PubMed DOI

Shaw W. H., Anderson J. W. (1974). The enzymology of adenosine triphosphate sulphurylase from spinach leaf tissue. Biochem. J. 139, 27–35. PubMed PMC

Shu L., Hu Z. (2012). Characterization and differential expression of microRNAs elicited by sulfur deprivation in PubMed DOI PMC

Song P., Li L., Liu J. (2013). Proteomic analysis in nitrogen-deprived PubMed DOI PMC

Suga H., Chen Z., de Mendoza A., Sebe-Pedros A., Brown M. W., Kramer E., et al. (2013). The PubMed DOI PMC

Sun M., Leyh T. S. (2006). Channeling in sulfate activating complexes. Biochemistry 45, 11304–11311. 10.1021/bi060421e PubMed DOI

Taguchi Y., Sugishima M., Fukuyama K. (2004). Crystal structure of a novel zinc-binding ATP sulfurylase from PubMed DOI

Takahashi H., Kopriva S., Giordano M., Saito K., Hell R. (2011). Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157–184. 10.1146/annurev-arplant-042110-103921 PubMed DOI

Ullrich T. C., Blaesse M., Huber R. (2001). Crystal structure of ATP sulfurylase from PubMed DOI PMC

Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., Von Ballmoos P., et al. (2002). Flux control of sulphate assimilation in PubMed DOI

Wang M., Wang Q., Zhang B. (2013). Response of miRNAs and their targets to salt and drought stresses in cotton ( PubMed DOI

Yatusevich R., Mugford S. G., Matthewman C., Gigolashvili T., Frerigmann H., Delaney S., et al. (2010). Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in PubMed DOI

Yildiz F. H., Davies J. P., Grossman A. R. (1996). Sulfur availability and the PubMed DOI PMC

Yu Z., Lansdon E. B., Segel I. H., Fisher A. J. (2007). Crystal structure of the bifunctional ATP sulfurylase - APS kinase from the chemolithotrophic thermophile PubMed DOI

Zhang Z., Shrager J., Jain M., Chang C. W., Vallon O., Grossman A. R. (2004). Insights into the survival of PubMed DOI PMC

Zhaxybayeva O., Gogarten J. P., Charlebois R. L., Doolittle W. F., Papke R. T. (2006). Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res. 16, 1099–1108. 10.1101/gr.5322306 PubMed DOI PMC

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