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. 1996 Oct;112(2):669–675. doi: 10.1104/pp.112.2.669

Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii.

F H Yildiz 1, J P Davies 1, A Grossman 1
PMCID: PMC157991  PMID: 8883379

Abstract

A Chlamydomonas reinhardtii adenosine triphosphate (ATP) sulfurylase cDNA clone (pATS1) was selected by complementing a mutation in the ATP sulfurylase gene (cysD) of Escherichia coli. E. coli cysD strains harboring pATS1 grow on medium containing sulfate as the sole sulfur source and exhibit ATP sulfurylase activity. The amino acid sequence of the C. reinhardtii ATP sulfurylase, derived from the nucleotide sequence of the complementing gene (ATS1), is 25 to 40% identical to that of ATP sulfurylases in other eukaryotic organisms and has a putative transit peptide at its amino terminus. ATP sulfurylase mRNA was present when cells were grown in sulfur-replete medium, but accumulated to higher levels when the cells were exposed to sulfur-limiting conditions. Furthermore, sulfur-stress-induced accumulation of the ATS1 transcript was reduced in a strain defective in SAC1, a gene that is critical for acclimation to sulfur-limited growth.

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Selected References

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  1. Borges-Walmsley M. I., Turner G., Bailey A. M., Brown J., Lehmbeck J., Clausen I. G. Isolation and characterisation of genes for sulphate activation and reduction in Aspergillus nidulans: implications for evolution of an allosteric control region by gene duplication. Mol Gen Genet. 1995 May 20;247(4):423–429. doi: 10.1007/BF00293143. [DOI] [PubMed] [Google Scholar]
  2. Davies J. P., Weeks D. P., Grossman A. R. Expression of the arylsulfatase gene from the beta 2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res. 1992 Jun 25;20(12):2959–2965. doi: 10.1093/nar/20.12.2959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Davies J. P., Yildiz F. H., Grossman A. Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J. 1996 May 1;15(9):2150–2159. [PMC free article] [PubMed] [Google Scholar]
  4. Foster B. A., Thomas S. M., Mahr J. A., Renosto F., Patel H. C., Segel I. H. Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum. Identification of a likely allosteric domain. J Biol Chem. 1994 Aug 5;269(31):19777–19786. [PubMed] [Google Scholar]
  5. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  6. Keegstra K. Transport and routing of proteins into chloroplasts. Cell. 1989 Jan 27;56(2):247–253. doi: 10.1016/0092-8674(89)90898-2. [DOI] [PubMed] [Google Scholar]
  7. Kuras L., Thomas D. Functional analysis of Met4, a yeast transcriptional activator responsive to S-adenosylmethionine. Mol Cell Biol. 1995 Jan;15(1):208–216. doi: 10.1128/mcb.15.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Leustek T., Murillo M., Cervantes M. Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae. Plant Physiol. 1994 Jul;105(3):897–902. doi: 10.1104/pp.105.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Levi A. S., Wolf G. Purification and properties of the enzyme ATP-sulfurylase and its relation to vitamin A. Biochim Biophys Acta. 1969 Apr 22;178(2):262–282. doi: 10.1016/0005-2744(69)90395-7. [DOI] [PubMed] [Google Scholar]
  10. Leyh T. S., Taylor J. C., Markham G. D. The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J Biol Chem. 1988 Feb 15;263(5):2409–2416. [PubMed] [Google Scholar]
  11. Li H., Deyrup A., Mensch J. R., Jr, Domowicz M., Konstantinidis A. K., Schwartz N. B. The isolation and characterization of cDNA encoding the mouse bifunctional ATP sulfurylase-adenosine 5'-phosphosulfate kinase. J Biol Chem. 1995 Dec 8;270(49):29453–29459. doi: 10.1074/jbc.270.49.29453. [DOI] [PubMed] [Google Scholar]
  12. Lunn J. E., Droux M., Martin J., Douce R. Localization of ATP Sulfurylase and O-Acetylserine(thiol)lyase in Spinach Leaves. Plant Physiol. 1990 Nov;94(3):1345–1352. doi: 10.1104/pp.94.3.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Marzluf G. A., Metzenberg R. L. Positive control by the cys-3 locus in regulation of sulfur metabolism in Neurospora. J Mol Biol. 1968 Apr 28;33(2):423–437. doi: 10.1016/0022-2836(68)90199-x. [DOI] [PubMed] [Google Scholar]
  14. Murillo M., Leustek T. Adenosine-5'-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5'-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch Biochem Biophys. 1995 Oct 20;323(1):195–204. doi: 10.1006/abbi.1995.0026. [DOI] [PubMed] [Google Scholar]
  15. Onajobi F. D., Cole C. V., Ross C. Adenosine 5'-triphosphate-sulfurylase in corn roots and its partial purification. Plant Physiol. 1973 Dec;52(6):580–584. doi: 10.1104/pp.52.6.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Osslund T., Chandler C., Segel I. H. ATP sulfurylase from higher plants : purification and preliminary kinetics studies on the cabbage leaf enzyme. Plant Physiol. 1982 Jul;70(1):39–45. doi: 10.1104/pp.70.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Paietta J. V., Akins R. A., Lambowitz A. M., Marzluf G. A. Molecular cloning and characterization of the cys-3 regulatory gene of Neurospora crassa. Mol Cell Biol. 1987 Jul;7(7):2506–2511. doi: 10.1128/mcb.7.7.2506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Paietta J. V. Production of the CYS3 regulator, a bZIP DNA-binding protein, is sufficient to induce sulfur gene expression in Neurospora crassa. Mol Cell Biol. 1992 Apr;12(4):1568–1577. doi: 10.1128/mcb.12.4.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Renosto F., Martin R. L., Borrell J. L., Nelson D. C., Segel I. H. ATP sulfurylase from trophosome tissue of Riftia pachyptila (hydrothermal vent tube worm). Arch Biochem Biophys. 1991 Oct;290(1):66–78. doi: 10.1016/0003-9861(91)90592-7. [DOI] [PubMed] [Google Scholar]
  20. Renosto F., Martin R. L., Wailes L. M., Daley L. A., Segel I. H. Regulation of inorganic sulfate activation in filamentous fungi. Allosteric inhibition of ATP sulfurylase by 3'-phosphoadenosine-5'-phosphosulfate. J Biol Chem. 1990 Jun 25;265(18):10300–10308. [PubMed] [Google Scholar]
  21. Schwedock J. S., Long S. R. Rhizobium meliloti genes involved in sulfate activation: the two copies of nodPQ and a new locus, saa. Genetics. 1992 Dec;132(4):899–909. doi: 10.1093/genetics/132.4.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schwedock J., Long S. R. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature. 1990 Dec 13;348(6302):644–647. doi: 10.1038/348644a0. [DOI] [PubMed] [Google Scholar]
  23. Shaw W. H., Anderson J. W. Purification, properties and substrate specificity of adenosine triphosphate sulphurylase from spinach leaf tissue. Biochem J. 1972 Mar;127(1):237–247. doi: 10.1042/bj1270237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shoyab M., Su L. Y., Marx W. Purification and properties of ATP-sulfurylase from Furth mouse mastocytoma. Biochim Biophys Acta. 1972 Jan 20;258(1):113–124. doi: 10.1016/0005-2744(72)90971-0. [DOI] [PubMed] [Google Scholar]
  25. Thomas D., Cherest H., Surdin-Kerjan Y. Elements involved in S-adenosylmethionine-mediated regulation of the Saccharomyces cerevisiae MET25 gene. Mol Cell Biol. 1989 Aug;9(8):3292–3298. doi: 10.1128/mcb.9.8.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thomas D., Jacquemin I., Surdin-Kerjan Y. MET4, a leucine zipper protein, and centromere-binding factor 1 are both required for transcriptional activation of sulfur metabolism in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Apr;12(4):1719–1727. doi: 10.1128/mcb.12.4.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yildiz F. H., Davies J. P., Grossman A. R. Characterization of Sulfate Transport in Chlamydomonas reinhardtii during Sulfur-Limited and Sulfur-Sufficient Growth. Plant Physiol. 1994 Mar;104(3):981–987. doi: 10.1104/pp.104.3.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yu M., Martin R. L., Jain S., Chen L. J., Segel I. H. Rat liver ATP-sulfurylase: purification, kinetic characterization, and interaction with arsenate, selenate, phosphate, and other inorganic oxyanions. Arch Biochem Biophys. 1989 Feb 15;269(1):156–174. doi: 10.1016/0003-9861(89)90096-9. [DOI] [PubMed] [Google Scholar]
  29. de Hostos E. L., Togasaki R. K., Grossman A. Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J Cell Biol. 1988 Jan;106(1):29–37. doi: 10.1083/jcb.106.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. von Heijne G., Steppuhn J., Herrmann R. G. Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem. 1989 Apr 1;180(3):535–545. doi: 10.1111/j.1432-1033.1989.tb14679.x. [DOI] [PubMed] [Google Scholar]

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