The role of 5′-adenylylsulfate reductase in the sulfur assimilation pathway of soybean: Molecular cloning, kinetic characterization, and gene expression

Phytochemistry

Volumn 69, Issue 2, 2008, Pages 356-364

  Phartiyal, Pallavi ^a   Kim, Won Seok ^a   Cahoon, Rebecca E ^b   Jez, Joseph M ^b   Krishnan, Hari B ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

5 Adenylyl reductase; APS reductase; Cloning; Cold stress; Glycine max; Kinetic analysis; Legume; Leguminosae; Nutrient stress; Seed development; Soybean; Sulfur

Indexed keywords

FABACEAE; GLYCINE MAX;

ADENYLYLSULFATE REDUCTASE; OXIDOREDUCTASE; SULFUR;

ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOME; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOLECULAR CLONING; PLANT SEED; SOYBEAN; TEMPERATURE;

CLONING, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; KINETICS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; SEEDS; SOYBEANS; SULFUR; TEMPERATURE;

EID: 37549006750     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2007.07.013     Document Type: Article

References (53)

1. Berendt U., Haverkamp T., Prior A., and Schwenn J.D. Reaction mechanism of thioredoxin: 3′-phosphoadenylsulfate reductase investigated by site-directed mutagenesis. Eur. J. Biochem. 233 (1995) 347-356
2. Bick J.A., and Leustek T. Plant sulfur metabolism: the reduction of sulfate to sulfite. Curr. Opin. Plant Biol. 1 (1998) 240-244
3. Bick J.A., Aslund F., Chen F., and Leustek T. Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylsulfate reductase. Proc. Natl. Acad. Sci. USA 95 (1998) 8404-8409
4. Bick J.A., Setterdahl A.T., Knaff D.B., Chen Y., Pitcher L.H., Zilinskas B.A., and Leustek T. Regulation of the plant-type 5'-adenylyl sulfate reductase by oxidative stress. Biochemistry 40 (2001) 9040-9048
5. Burton J.W. Soybean. Field Crops Res. 53 (1997) 171-186
6. Burton J.W., Purcell A.E., and Walter J.W.M. Methionine concentration in soybean protein from populations selected for increased percent protein. Crop Sci. 22 (1982) 430-432
7. Carroll K.S., Gao H., Chen H., Stout C.D., Leary J.A., and Bertozzi C.R. A conserved mechanism for sulfonucleotide reduction. PLOS Biol. 3 (2005) e250
8. Chronis D., and Krishnan H.B. Sulfur assimilation in soybean (Glycine max[L.]Merr) molecular cloning and characterization of O-acetylserine (thiol) lyase. Crop Sci. 43 (2003) 1819-1827
9. Chronis D., and Krishnan H.B. Sulfur assimilation in soybean (Glycine max [L.]Merr): molecular cloning and characterization of a cytosolic isoform of serine acetyltransferase. Planta 218 (2004) 417-426
10. Cleland W.W. Statistical analysis of enzyme kinetic data. Methods Enzymol. 63 (1979) 103-138
11. Emanuelsson O., Nielsen H., and von Heijne G. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8 (1999) 978-984
12. Essigmann B., Guler S., Narang R.A., Linke D., and Benning C. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95 (1998) 1950-1955
13. Giovanelli J., Mudd S.H., and Datko A.H. Sulfur amino acids in plants. In: Miflin B.J. (Ed). The Biochemistry of Plants (1980), Academic Press, New York 454-500
14. Gutierrez-Marcos J.F., Roberts M.A., Campbell E.I., and Wray J.L. 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. Proc. Natl. Acad. Sci. USA 93 (1996) 13377-13382
15. Hartmann T., Mult S., Suter M., Rennenberg H., and Herschbach C. Leaf-age dependent differences in sulfur assimilation and allocation in poplar (Populus tremula x P. alba) leaves. J. Exp. Bot. 51 (2000) 1077-1088
16. Hawkesford M.J. Plant responses to sulfur deficiency and the genetic manipulation of sulfate transporters to improve S-utilization efficiency. J. Exp. Bot. 51 (2000) 131-138
17. Heiss S., Schafer H.J., Haag-Kerwer A., and Rausch T. Cloning sulfur assimilation genes of Brassica juncea L: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol. Biol. 39 (1999) 847-857
18. Hell R. Molecular physiology of plant sulfur metabolism. Planta 202 (1997) 138-148
19. Herrin D.L., and Schmidt G.W. Rapid, reversible staining of northern blots prior to hybridization. Biotechniques 6 (1988) 196-200
20. Hesse H., Trachsel N., Suter M., Kopriva S., von Ballmoos P., Rennenberg H., and Brunold C. Effect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J. Exp. Bot. 54 (2003) 1701-1709
21. Hofgen R., Kreft O., Willmitzer L., and Hesse H. Manipulation of thiol contents in plants. Amino Acids 20 (2001) 291-299
22. Hopkins L., Parmar S., Bouranis D.L., Howarth J.R., and Hawkesford M.J. Coordinated expression of sulfate uptake and components of the sulfate assimilatory pathway in maize. Plant Biol. 6 (2004) 408-414
23. Kocsy G., von Ballmoos P., Suter M., Rüegsegger A., Galli U., Szalai G., Galiba G., and Brunold C. Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211 (2000) 528-536
24. Kocsy G., von Ballmoos P., Rüegsegger A., Szalai G., Galiba G., and Brunold C. Increasing the glutathione content in a chilling-sensitive maize genotype using safeners increased protection against chilling-induced injury. Plant Physiol. 127 (2001) 1147-1156
25. Kopriva S., and Koprivova A. Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J. Exp. Bot. 55 (2004) 1775-1783
26. Kopriva S., Buchert T., Fritz G., Suter M., Weber M., Benda R., Schaller J., Feller U., Schurmann P., Schunemann V., Trautwein A.X., Kroneck P.M., and Brunold C. Plant adenosine 5'-phosphosulfate reductase is a novel iron-sulfur protein. J. Biol. Chem. 276 (2001) 42881-42886
27. Kopriva S., Suter M., von Ballmoos P., Hesse H., Krahenbuhl U., Rennenberg H., and Brunold C. Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol. 130 (2002) 1406-1413
28. Koprivova A., Suter M., den Camp R.O., Brunold C., and Kopriva S. Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol. 122 (2000) 737-746
29. Krishnan H.B. Engineering soybean for enhanced sulfur amino acid content. Crop Sci. 45 (2005) 454-461
30. Leustek T., and Saito K. Sulfate transport and assimilation in plants. Plant Physiol. 120 (1997) 637-643
31. Leustek T., Martin M.N., Bick J.A., and Davies D.P. Pathway and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 51 (2000) 141-165
32. Martin M.N., Tarczynski M.C., Shen B., and Leustek T. The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth. Res. 86 (2005) 309-323
33. Nakai K., and Kanehisa M. Expert system for predicting protein localization sites in gram-negative bacteria. Proteins 11 (1991) 105-110
34. Ohkama N., Takei K., Sakakibara H., Hayashi H., Yoneyama T., and Fujiwara T. Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43 (2002) 1493-1501
35. Park K.H., and Kanehisa M. Prediction of protein subcellular locations by support vector machines using compositions of amino acids and amino acid pairs. Bioinformatics 19 (2003) 1656-1663
36. Phartiyal P., Kim W.S., Cahoon R.E., Jez J.M., and Krishnan H.B. Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch. Biochem. Biophys. 450 (2006) 20-29
37. Reuveny Z., Dougall D.K., and Trinity P.M. Regulatory coupling of nitrate and sulfate assimilation pathways in cultured tobacco cells. Proc. Natl. Acad. Sci. USA 11 (1980) 6670-6672
38. Rotte C., and Leustek T. Differential subcellular localization and expression of ATP sulfurylase and 5'-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol. 124 (2000) 715-724
39. Schachtman D.P., and Shin R. Nutrient Sensing and Signaling: NPKS. Annu. Rev. Plant Biol. 58 (2007) 47-69
40. Schmidt A., and Jäger K. Open questions about sulfur metabolism in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 (1992) 325-349
41. Schmutz D., and Brunold C. Regulation of sulfate assimilation in Plants XIII: assimilatory sulfate reduction during ontogenesis of primary leaves of Phaseolus vulgaris L. Plant Physiol. 70 (1982) 524-527
42. Schnug E. Significance of sulfur for the quality of domesticated plants. In: Cram W.J., DeKok L.J., Stulen I., Brunold C., and Rennenberg H. (Eds). Sulphur Metabolism in Higher Plants (1997), Backhuys Publishing, Netherlands 109-130
43. Segal I.H. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems (1975), John Wiley & Sons, Inc, New York
44. Setya A., Murillo M., and Leustek T. Sulfate reduction in higher plants: molecular evidence for a novel 5'-adenylsulfate reductase. Proc. Natl. Acad. Sci. USA 93 (1996) 13383-13388
45. Sexton P.J., and Shibles R.M. Activity of ATP sulfurylase in reproductive soybean. Crop Sci. 39 (1999) 131-135
46. 35S]-sulfate to roots during vegetative growth of soybean. Plant Physiol. 110 (1996) 1151-1157
47. Suter M., van Ballmoon P., Kopriva S., den Camp R.O., Schaller J., Kuhlemeier C., Schürman P., and Brunold C. Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes. J. Biol. Chem. 275 (2000) 930-936
48. Tabe L.M., and Droux M. Sulfur assimilation in developing lupin cotyledons could contribute significantly to the accumulation of organic sulfur reserves in the seed. Plant Physiol. 126 (2001) 176-187
49. Takahashi H., Yamazaki M., Sasakura N., Watanabe A., Leustek T., Engler J.A., Engler G., van Montagu M., and Saito K. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94 (1997) 11102-11107
50. Tsakraklides G., Martin M., Chalam R., Tarczynski M.C., Schmidt A., and Leustek T. Sulphate reduction is increased in transgenic Arabidopsis thaliana expressing adenylylsulphate reductase from Pseudomonas aeruginosa. Plant J. 32 (2002) 879-889
51. Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., van Ballmoos P., Krähenbühl U., den Camp R.O., and Brunold C. Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulfurylase to negative control by thiols. Plant J. 31 (2002) 729-740
52. 2S and cysteine. Physiol. Plant. 67 (1986) 81-86
53. Yamaguchi Y., Nakamura T., Harada E., Koizumi N., and Sano H. Differential accumulation of transcripts encoding sulfur assimilation enzymes upon sulfur and/or nitrogen deprivation in Arabidopsis thaliana. Biosci. Biotech. Biochem. 4 (1999) 762-766