Abstract
Sulfate assimilation provides reduced sulfur for the synthesis of the amino acids cysteine and methionine and for a range of other metabolites. The key step in control of plant sulfate assimilation is the reduction of adenosine 5′-phosphosulfate to sulfite. The enzyme catalyzing this reaction, adenosine 5′phosphosulfate reductase (APR), is found as an iron sulfur protein in plants, algae, and many bacteria. In the moss Physcomitrella patens, however, a novel isoform of the enzyme, APR-B, has recently been discovered lacking the co-factor. To assess the function of the novel APR-B we used homologous recombination to disrupt the corresponding gene in P. patens. The knock-out plants were able to grow on sulfate as a sole sulfur source and the content of low molecular weight thiols was not different from wild type plants or plants where APR was disrupted. However, when treated with low concentrations of cadmium the APR-B knockout plants were more sensitive than both wild type and APR knockouts. In wild type P. patens, the two APR isoforms were not affected by treatments that strongly regulate this enzyme in flowering plants. The data thus suggest that in P. patens APS reduction is not the major control step of sulfate assimilation.
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References
Bick J-A, Åslund F, Chen Y, Leustek T (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 95:8404–8409
Bick JA, Seterdahl AT, Knaff DB, Chen YC, Pitcher LH, Zilinskas BA, Leustek T (2001) Regulation of the plant-type 5′-adenylyl sulfate reductase by oxidative stress. Biochemistry 40:9040–9048
Brunner M, Kocsy G, Ruegsegger A, Schmutz D. Brunold C (1995) Effect of chilling on assimilatory sulphate reduction and glutathione synthesis in maize. J Plant Physiol 146:743–747
Bierfreund NM, Tintelnot S, Reski R, Decker EL (2004) Loss of GH3-function does not affect phytochrome-mediated development in a moss, Physcomitrella patens. J Plant Physiol 161:823–835
Frank W, Decker EL, Reski R (2005a) Molecular tools to study Physcomitrella patens. Plant Biol 7:220–227
Frank W, Ratnadewi D Reski R (2005b) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220:384–394
Girke T, Schmidt H, Zäringer U, Reski R, Heinz E (1998) Identification of a novel Delta 6 acyl-group desaturase by targeted gene disruption in Physcomitrella patens. Plant J 15:39–48
Hohe A, Decker EL, Gorr G, Schween G, Reski R (2002) Tight control of growth and cell differentiation in photoautotrophically growing moss Physcomitrella patens bioreactor cultures. Plant Cell Rep 20:1135–1140
Hohe A, Egener T, Lucht J, Holtorf H, Reinhard C, Schween G, Reski R (2004) An improved and highly standardised transformation procedure allows efficient production of single and multiple targeted gene knockouts in a moss, Physcomitrella patens. Curr Genet 44:339–347
Kamisugi Y, Schlink K, Rensing SA, Schween G, Stackelberg M v, Cuming AC, Reski R, Cove DJ (2006) The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucl Acids Res 34:6205–6214
Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495
Kopriva S, Koprivova A (2004) Plant adenosine 5′phosphosulfate reductase—the past, the present, and the future. J Exp Bot 55:1775–1783
Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842
Kopriva S, Büchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schürmann P, Schünemann V, Trautwein AX, Kroneck PMH, Brunold C (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron–sulfur protein. J Biol Chem 276:42881–42886
Kopriva S, Büchert T, Fritz G, Suter M, Benda R, Schünemann V, Koprivova A, Schürmann P, Trautwein AX, Kroneck PMH, Brunold C (2002a) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation. J Biol Chem 277:21786–21791
Kopriva S, Suter M, von Ballmoos P, Hesse H, Krähenbühl U, Rennenberg H, Brunold C (2002b) Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol 130:1406–1413
Kopriva S, Fritzemeier K, Wiedemann G, Reski R (2007a) The putative moss 3′phosphoadenosine 5′phosphosulfate reductase is a novel form of adenosine 5′phosphosulfate reductase without iron sulfur cluster. J Biol Chem 282:22930–22938
Kopriva S, Wiedemann G, Reski R (2007b) Sulfate assimilation in basal land plants—what does genomic sequencing tell us? Plant Biol. doi:10.1055/s-2007-965430
Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746
Koprivova A, Meyer A, Schween G, Herschbach C, Reski R, Kopriva S (2002) Functional knockout of the adenosine 5´phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation. J Biol Chem 277:32195–32201
Koprivova A, Stemmer C, Altmann F, Hoffmann A, Kopriva S, Gorr G, Reski R, Decker EL (2004) Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans. Plant Biotechnol J 2:517–523
Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, 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
Lee SM, Leustek T (1999) The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141:201–207
Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165
Li JY, Schiff JA (1991) Purification and properties of adenosine 5′-phosphosulphate sulphotransferase from Euglena. Biochem J 274:355–360
Reski R, Abel WO (1985) Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165:354–358
Reski R, Reynolds S, Wehe M, Kleber-Janke T, Kruse S (1998) Moss (Physcomitrella patens) expressed sequence tags include several sequences which are novel for plants. Bot Acta 111:145–151
Rother M, Krauss GJ, Grass G, Wesenberg D (2006) Sulphate assimilation under Cd2+ stress in Physcomitrella patens—combined transcript, enzyme and metabolite profiling. Plant Cell Environ 29:1801–1811
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sato N, Nakayama M, Hase T (2001) The 70-kDa major DNA—compacting protein of the chloroplast nucleoid is sulfite reductase. FEBS Lett 487:347–350
Schaefer DG (2001) Gene targeting in Physcomitrella patens. Curr Opin Plant Biol 4:143–150
Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylsulfate reductase. Proc Natl Acad Sci USA 93:13383–13388
Strepp R, Scholz S, Kruse S, Speth V, Reski R (1998) Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci USA 95:4368–4373
Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos O, Krähenbuhl U, Op den Camp R, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible to negative control by thiols than ATP sulphurylase. Plant J 31:729–740
Westerman S, Stulen I, Suter M, Brunold C, De Kok LJ (2001) Atmospheric H2S as sulphur source for Brassica oleracea: consequences for the activity of the enzymes of the assimilatory sulphate reduction pathway. Plant Physiol Biochem 39:425–432
Acknowledgements
This work was supported by the German Research Council (DFG) grant KO2065/3 within the research group FOR 383 “Sulfur metabolism in plants: junction of basic metabolic pathways and molecular mechanisms of stress resistance”. We thank Anne Katrin Prowse for help with the manuscript.
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Wiedemann, G., Koprivova, A., Schneider, M. et al. The role of the novel adenosine 5′-phosphosulfate reductase in regulation of sulfate assimilation of Physcomitrella patens . Plant Mol Biol 65, 667–676 (2007). https://doi.org/10.1007/s11103-007-9231-2
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DOI: https://doi.org/10.1007/s11103-007-9231-2