PATHWAYS AND REGULATION OF SULFUR METABOLISM REVEALED THROUGH MOLECULAR AND GENETIC STUDIES.

Sulfur is essential for life. Its oxidation state is in constant flux as it circulates through the global sulfur cycle. Plants play a key role in the cycle since they are primary producers of organic sulfur compounds. They are able to couple photosynthesis to the reduction of sulfate, assimilation into cysteine, and further metabolism into methionine, glutathione, and many other compounds. The activity of the sulfur assimilation pathway responds dynamically to changes in sulfur supply and to environmental conditions that alter the need for reduced sulfur. Molecular genetic analysis has allowed many of the enzymes and regulatory mechanisms involved in the process to be defined. This review focuses on recent advances in the field of plant sulfur metabolism. It also emphasizes areas about which little is known, including transport and recycling/degradation of sulfur compounds.

[1]  J. Slovin,et al.  Purified gamma-glutamyl transpeptidases from tomato exhibit high affinity for glutathione and glutathione S-conjugates. , 2000, Plant physiology.

[2]  P. von Ballmoos,et al.  Adenosine 5′-Phosphosulfate Sulfotransferase and Adenosine 5′-Phosphosulfate Reductase Are Identical Enzymes* , 2000, The Journal of Biological Chemistry.

[3]  T. Leustek,et al.  Identification of a New Class of 5′-Adenylylsulfate (APS) Reductases from Sulfate-Assimilating Bacteria , 2000, Journal of bacteriology.

[4]  K. Nakamura,et al.  Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Kazuki Saito,et al.  Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform , 1999 .

[6]  S. Kopriva,et al.  Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. , 1999, The Plant journal : for cell and molecular biology.

[7]  M. Hirai,et al.  Role of O-acetyl-l-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition , 1999, Planta.

[8]  B. Kloareg,et al.  Sulfated Oligosaccharides Mediate the Interaction between a Marine Red Alga and Its Green Algal Pathogenic Endophyte , 1999, The Plant Cell.

[9]  M. J. Pimenta,et al.  S-Methylmethionine Plays a Major Role in Phloem Sulfur Transport and Is Synthesized by a Novel Type of Methyltransferase , 1999, Plant Cell.

[10]  G. Adam,et al.  Inactivation of Brassinosteroid Biological Activity by a Salicylate-inducible Steroid Sulfotransferase from Brassica napus * , 1999, The Journal of Biological Chemistry.

[11]  T. Leustek,et al.  Sulfate transport and assimilation in plants , 1999, Plant physiology.

[12]  A. Wellburn,et al.  Elevated Glutathione Biosynthetic Capacity in the Chloroplasts of Transgenic Tobacco Plants Paradoxically Causes Increased Oxidative Stress , 1999, Plant Cell.

[13]  J. Schroeder,et al.  Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast , 1999, The EMBO journal.

[14]  P. A. Rea,et al.  AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Kloareg,et al.  Oligosaccharide recognition signals and defence reactions in marine plant-microbe interactions. , 1999, Current opinion in microbiology.

[16]  A. Grossman,et al.  Sac3, an Snf1-like Serine/Threonine Kinase That Positively and Negatively Regulates the Responses of Chlamydomonas to Sulfur Limitation , 1999, Plant Cell.

[17]  C. Cobbett,et al.  Phytochelatin Synthase Genes from Arabidopsis and the Yeast Schizosaccharomyces pombe , 1999 .

[18]  B. Touraine,et al.  Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. , 1999, The Plant journal : for cell and molecular biology.

[19]  Jon Beckwith,et al.  Bridge over Troubled Waters Sensing Stress by Disulfide Bond Formation , 1999, Cell.

[20]  T. Leustek,et al.  The affect of cadmium on sulfate assimilation enzymes in Brassica juncea , 1999 .

[21]  A. Wiesmann,et al.  Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures. , 1999, Biochimica et biophysica acta.

[22]  D. Ferrington,et al.  Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. , 1999, Biochemistry.

[23]  M. Hawkesford,et al.  Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth , 1998, Plant physiology.

[24]  M. Lieberman,et al.  γ-Glutamyl Leukotrienase, a γ-Glutamyl Transpeptidase Gene Family Member, Is Expressed Primarily in Spleen* , 1998, The Journal of Biological Chemistry.

[25]  C. Cobbett,et al.  The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. , 1998, The Plant journal : for cell and molecular biology.

[26]  U. Berger,et al.  Characterization of a Rat Na+-Dicarboxylate Cotransporter* , 1998, The Journal of Biological Chemistry.

[27]  T. Leustek,et al.  Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5'-adenylylsulfate reductase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Job,et al.  Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants--structural and kinetic properties of the free and bound enzymes. , 1998, European journal of biochemistry.

[29]  S. Ravanel,et al.  The specific features of methionine biosynthesis and metabolism in plants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  T. Leustek,et al.  APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme. , 1998, Biochemical and biophysical research communications.

[31]  T. Leustek,et al.  Plant sulfur metabolism--the reduction of sulfate to sulfite. , 1998, Current opinion in plant biology.

[32]  P. A. Rea,et al.  FROM VACUOLAR GS-X PUMPS TO MULTISPECIFIC ABC TRANSPORTERS. , 1998, Annual review of plant physiology and plant molecular biology.

[33]  C. Bork,et al.  Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. , 1998, Gene.

[34]  A. Grossman,et al.  The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. , 1998, Plant physiology.

[35]  M. Matzuk,et al.  Leukotriene D4 and cystinyl-bis-glycine metabolism in membrane-bound dipeptidase-deficient mice. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  L. Jouanin,et al.  Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants , 1998 .

[37]  M. May Review article. Glutathione homeostasis in plants: implications for environmental sensing and plant development , 1998 .

[38]  Mike J. May,et al.  Glutathione homeostasis in plants: implications for environmental sensing and plant development , 1998 .

[39]  G. Noctor Review article. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants , 1998 .

[40]  M. Suter,et al.  Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves , 1998, Plant physiology.

[41]  Y. Matsubayashi,et al.  Phytosulfokine-alpha, a sulfated pentapeptide, stimulates the proliferation of rice cells by means of specific high- and low-affinity binding sites. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[42]  H. Lambers,et al.  SO42- Deprivation Has an Early Effect on the Content of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase and Photosynthesis in Young Leaves of Wheat , 1997, Plant physiology.

[43]  F. W. Smith,et al.  Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. , 1997, The Plant journal : for cell and molecular biology.

[44]  J. Lafontaine,et al.  The enzyme involved in sulfation of the turgorin, gallic acid 4-O-(beta-D-glucopyranosyl-6'-sulfate) is pulvini-localized in Mimosa pudica. , 1997, The Plant journal : for cell and molecular biology.

[45]  Roughan Pg,et al.  Stromal concentrations of coenzyme A and its esters are insufficient to account for rates of chloroplast fatty acid synthesis: evidence for substrate channelling within the chloroplast fatty acid synthase. , 1997 .

[46]  M. Van Montagu,et al.  Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[47]  P. A. Rea,et al.  AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Cho,et al.  Differential expression of two functional serine/threonine protein kinases from soyabean that have an unusual acidic domain at the carboxy terminus , 1997, Molecular and General Genetics MGG.

[49]  P. A. Rea,et al.  Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. , 1997, Phytochemistry.

[50]  F. Marsolais,et al.  Biochemistry and molecular biology of plant sulfotransferases , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[51]  J. Anderson,et al.  Allocation of S in Generative Growth of Soybean , 1997, Plant physiology.

[52]  Y. Suzuki,et al.  Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[53]  B. Goldman,et al.  Molecular and immunological analysis of an ABC transporter complex required for cytochrome c biogenesis. , 1997, Journal of molecular biology.

[54]  M. Lieberman,et al.  Metabolism of Leukotriene C4 in γ-Glutamyl Transpeptidase-deficient Mice* , 1997, The Journal of Biological Chemistry.

[55]  R. Hell,et al.  Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. , 1997, The Plant journal : for cell and molecular biology.

[56]  J. Wray,et al.  Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and "APS reductase" activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Setya,et al.  Sulfate reduction in higher plants: molecular evidence for a novel 5'-adenylylsulfate reductase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[58]  A. Grossman,et al.  Sulfur Availability and the SAC1 Gene Control Adenosine Triphosphate Sulfurylase Gene Expression in Chlamydomonas reinhardtii , 1996, Plant physiology.

[59]  Hideki Takahashi,et al.  Isolation and characterization of a cDNA encoding a sulfate transporter from Arabidopsis thaliana , 1996, FEBS letters.

[60]  L. Hooper,et al.  From legumes to leukocytes: biological roles for sulfated carbohydrates , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[61]  S. Delrot,et al.  Characterization of Glutathione Uptake in Broad Bean Leaf Protoplasts , 1996, Plant physiology.

[62]  Yi Wang,et al.  Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  M. Lieberman,et al.  Four Distinct Membrane-bound Dipeptidase RNAs Are Differentially Expressed and Show Discordant Regulation with γ-Glutamyl Transpeptidase* , 1996, The Journal of Biological Chemistry.

[64]  K. Marrs THE FUNCTIONS AND REGULATION OF GLUTATHIONE S-TRANSFERASES IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[65]  A. Grossman,et al.  Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. , 1996, The EMBO journal.

[66]  B. Touraine,et al.  Demand-Driven Control of Root ATP Sulfurylase Activity and SO42- Uptake in Intact Canola (The Role of Phloem-Translocated Glutathione) , 1996, Plant physiology.

[67]  P. Schröder,et al.  Degradation of glutathione S‐conjugates by a carboxypeptidase in the plant vacuole , 1996, FEBS letters.

[68]  G. Stacey,et al.  Cloning of a Second Arabidopsis Peptide Transport Gene , 1996, Plant physiology.

[69]  W. E. Rauser Phytochelatins and Related Peptides (Structure, Biosynthesis, and Function) , 1995, Plant physiology.

[70]  E. Belles-Boix,et al.  Characterization of Arabidopsis thaliana cDNAs that render yeasts tolerant toward the thiol-oxidizing drug diamide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[71]  D. Blanchard,et al.  The electronic plant gene register , 1995, Plant physiology.

[72]  J. Cohen,et al.  A New 1-Aminocyclopropane-1-Carboxylic Acid-Conjugating Activity in Tomato Fruit , 1995, Plant physiology.

[73]  T. Haverkamp,et al.  Reaction mechanism of thioredoxin: 3'-phospho-adenylylsulfate reductase investigated by site-directed mutagenesis. , 1995, European journal of biochemistry.

[74]  M. Murillo,et al.  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. , 1995, Archives of biochemistry and biophysics.

[75]  P. A. Rea,et al.  1-Chloro-2,4-Dinitrobenzene-Elicited Increase in Vacuolar Glutathione-S-Conjugate Transport Activity , 1995, Plant physiology.

[76]  N. Vermeulen,et al.  Enzymes and transport systems involved in the formation and disposition of glutathione S-conjugates. Role in bioactivation and detoxication mechanisms of xenobiotics. , 1995, Pharmacological reviews.

[77]  V. Walbot,et al.  A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2 , 1995, Nature.

[78]  C. Cobbett,et al.  Cadmium-Sensitive, cad1 Mutants of Arabidopsis thaliana Are Phytochelatin Deficient , 1995, Plant physiology.

[79]  A. Pajor Sequence and Functional Characterization of a Renal Sodium/Dicarboxylate Cotransporter (*) , 1995, The Journal of Biological Chemistry.

[80]  D. Keppler,et al.  The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. , 1994, The Journal of biological chemistry.

[81]  K. Saito,et al.  Modulation of Cysteine Biosynthesis in Chloroplasts of Transgenic Tobacco Overexpressing Cysteine Synthase [O-Acetylserine(thiol)-Iyase] , 1994, Plant physiology.

[82]  C. Gaillard,et al.  A herbicide antidote (safener) induces the activity of both the herbicide detoxifying enzyme and of a vacuolar transporter for the detoxified herbicide , 1994, FEBS letters.

[83]  J. Lancaster,et al.  Characterization of purified γ-glutamyl transpeptidase in onions: Evidence for in vivo role as a peptidase , 1994 .

[84]  H. Rennenberg,et al.  Influence of glutathione (GSH) on net uptake of sulphate and sulphate transport in tobacco plants , 1994 .

[85]  L. Willmitzer,et al.  Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant. , 1994, The Plant journal : for cell and molecular biology.

[86]  W. Frommer,et al.  Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters , 1994, FEBS letters.

[87]  A. Grossman,et al.  Characterization of Sulfate Transport in Chlamydomonas reinhardtii during Sulfur-Limited and Sulfur-Sufficient Growth , 1994, Plant physiology.

[88]  A. Grossman,et al.  Mutants of Chlamydomonas with Aberrant Responses to Sulfur Deprivation. , 1994, The Plant cell.

[89]  H. C. Patel,et al.  ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. , 1993, Archives of biochemistry and biophysics.

[90]  E. Grill,et al.  ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants , 1993, Nature.

[91]  T. Ishikawa,et al.  The ATP-dependent glutathione S-conjugate export pump. , 1992, Trends in biochemical sciences.

[92]  M. Walker-Simmons,et al.  Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[93]  M. Hirai,et al.  Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. , 1992, Plant physiology.

[94]  A. Teixeira,et al.  Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. , 1992, The Journal of biological chemistry.

[95]  U. Neuenschwander,et al.  Regulation of Sulfate Assimilation by Light and O-Acetyl-l-Serine in Lemna minor L. , 1991, Plant physiology.

[96]  A. Grossman,et al.  Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport , 1991, Journal of bacteriology.

[97]  A. Grossman,et al.  Isolation and characterization of a sulfur-regulated gene encoding a periplasmically localized protein with sequence similarity to rhodanese , 1991, Journal of bacteriology.

[98]  J. Lunn,et al.  Localization of ATP Sulfurylase and O-Acetylserine(thiol)lyase in Spinach Leaves. , 1990, Plant physiology.

[99]  J. Lai,et al.  High-affinity transport of glutathione is part of a multicomponent system essential for mitochondrial function. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[100]  Philippe Roche,et al.  Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal , 1990, Nature.

[101]  A. Meister Glutathione metabolism and its selective modification. , 1988, The Journal of biological chemistry.

[102]  L. Romero,et al.  Intracellular Levels and Regulation of O-Acetyl-L-Serine Sulfhydrylase Activity in Chlamydomonas reinhardtii , 1988 .

[103]  A. Grossman,et al.  Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii , 1988, The Journal of cell biology.

[104]  M. Carlson,et al.  A yeast gene that is essential for release from glucose repression encodes a protein kinase. , 1986, Science.

[105]  T. Kohchi,et al.  Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA , 1986, Nature.

[106]  K. Gayler,et al.  Effects of nutritional stress on the storage proteins of soybeans. , 1985, Plant physiology.

[107]  H. Rennenberg,et al.  Degradation of Glutathione in Plant Cells: Evidence against the Participation of a γ-Glutamyltranspeptidase , 1985 .

[108]  H. Rennenberg,et al.  γ‐Glutamylcyclotransferase in tobacco suspension cultures: Catalytic properties and subcellular localization , 1984 .

[109]  M. Carlson,et al.  Cloning and genetic mapping of SNF1, a gene required for expression of glucose-repressible genes in Saccharomyces cerevisiae , 1984, Molecular and cellular biology.

[110]  J. T. Madison,et al.  Exogenous methionine depresses level of mRNA for a soybean storage protein. , 1983, Biochemical and biophysical research communications.

[111]  H. Rennenberg,et al.  5-Oxo-prolinase in Nicotiana tabacum: catalytic properties and subcellular localization , 1981 .

[112]  R. Douce,et al.  Transport du sulfate à travers la double membrane limitante, ou enveloppe, des chloroplastes d'épinard , 1980 .

[113]  P. Filner,et al.  Regulation of adenosine triphosphate sulfurylase in cultured tobacco cells. Effects of sulfur and nitrogen sources on the formation and decay of the enzyme. , 1977, The Journal of biological chemistry.

[114]  M. Steine,et al.  Purification of a derepressible arylsulfatase from Chlamydomonas reinhardti. Properties of the enzyme in intact cells and in purified state. , 1975, Biochimica et biophysica acta.

[115]  J. Schiff,et al.  The Metabolism of Sulfate , 1973 .

[116]  H. Rennenberg,et al.  Sulfur Nutrition and Sulfur Assimilation in Higher Plants: Molecular, Biochemical and Physiological Aspects , 2000 .

[117]  J. Papenbrock,et al.  Characterization of a sulfurtransferase from Arabidopsis thaliana. , 2000, European journal of biochemistry.

[118]  E. Stadtman,et al.  Methionine sulfoxide reductase in antioxidant defense. , 1999, Methods in enzymology.

[119]  N. Koizumi,et al.  Differential accumulation of transcripts encoding sulfur assimilation enzymes upon sulfur and/or nitrogen deprivation in Arabidopsis thaliana. , 1999, Bioscience, biotechnology, and biochemistry.

[120]  M. Montagu,et al.  A cDNA encoding cinnamoyl-CoA reductase from Populus trichocarpa (accession no. AJ224986) , 1998 .

[121]  R. Hell Molecular physiology of plant sulfur metabolism , 1997, Planta.

[122]  M. Zenk Heavy metal detoxification in higher plants--a review. , 1996, Gene.

[123]  G. F. Ames,et al.  ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. , 1993, Annual review of microbiology.

[124]  A. Schmidt,et al.  Open Questions about Sulfur Metabolism in Plants , 1992 .

[125]  H. Rennenberg,et al.  Reduced glutathione (GSH) transport into cultured tobacco cells , 1992 .

[126]  J. Vega,et al.  Separation and regulatory properties of O-acetyl-L-serine sulfhydrylase isoenzymes from Chlamydomonas reinhardtii , 1991 .

[127]  R. H. Shimabukuro,et al.  GLUTATHIONE AND GLUCOSIDE CONJUGATION IN HERBICIDE SELECTIVITY , 1991 .

[128]  A. Datko,et al.  Sulfur Amino Acids in Plants , 1980 .

[129]  F. Schlenk The chemistry of biological sulfonium compounds. , 1965, Fortschritte der Chemie organischer Naturstoffe = Progress in the chemistry of organic natural products. Progres dans la chimie des substances organiques naturelles.