Sulfite reductase protects plants against sulfite toxicity

Plant Physiology

Volumn 161, Issue 2, 2013, Pages 725-743

  Yarmolinsky, Dmitry ^a   Brychkova, Galina ^a   Fluhr, Robert ^b   Sagi, Moshe ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873259759     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.207712     Document Type: Article

References (50)

1. Armengaud J, Gaillard J, Forest E, Jouanneau Y (1995) Characterization of a 2[4Fe-4S] ferredoxin obtained by chemical insertion of the Fe-S clusters into the apoferredoxin II from Rhodobacter capsulatus. Eur J Biochem 231: 396-404
2. Björkman M, Klingen I, Birch AN, Bones AM, Bruce TJ, Johansen TJ, Meadow R, Mølmann J, Seljåsen R, Smart LE, et al (2011) Phytochemicals of Brassicaceae in plant protection and human health: influences of climate, environment and agronomic practice. Phytochemistry 72: 538-556
3. Bork C, Schwenn JD, Hell R (1998) Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. Gene 212: 147-153
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
5. Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50: 696-709
6. Brychkova G, Yarmolinsky D, Fluhr R, Sagi M (2012a) The determination of sulfite levels and its oxidation in plant leaves. Plant Sci 190: 123-130
7. Brychkova G, Yarmolinsky D, Ventura Y, Sagi M (2012b) A novel in-gel assay and an improved kinetic assay for determining in vitro sulfite reductase activity in plants. Plant Cell Physiol 53: 1507-1516
8. Cannon GC, Ward LN, Case CI, Heinhorst S (1999) The 68 kDa DNA compacting nucleoid protein from soybean chloroplasts inhibits DNA synthesis in vitro. Plant Mol Biol 39: 835-845
9. Chi-Ham CL, Keaton MA, Cannon GC, Heinhorst S (2002) The DNAcompacting protein DCP68 from soybean chloroplasts is ferredoxin: sulfite reductase and co-localizes with the organellar nucleoid. Plant Mol Biol 49: 621-631
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hänsch R, Mendel RR (2001) Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase: a new player in plant sulfur metabolism. J Biol Chem 276: 46989-46994
12. Habuchi S, Ando R, Dedecker P, Verheijen W, Mizuno H, Miyawaki A, Hofkens J (2005) Reversible single-molecule photoswitching in the GFPlike fluorescent protein Dronpa. Proc Natl Acad Sci USA 102: 9511-9516
13. Hänsch R, Mendel RR (2008) Sulfite oxidation in plants. In Govindjee, J Amesz, J Barber, RE Blankenship, N Murata, WL Ogren, DR Ort, eds, Sulfur Metabolism in Phototrophic Organisms, Vol 27. Springer, Dordrecht, The Netherlands, pp 223-230
14. Hopkins RJ, van Dam NM, van Loon JJ (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54: 57-83
15. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747
16. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
17. Kang YW, Lee JY, Jeon Y, Cheong GW, Kim M, Pai HS (2010) In vivo effects of NbSiR silencing on chloroplast development in Nicotiana benthamiana. Plant Mol Biol 72: 569-583
18. Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hänsch R, Mendel RR, Meyer AJ, et al (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22: 1216-1231
19. Kisker C, Schindelin H, Rees DC (1997) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66: 233-267
20. Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot (Lond) 97: 479-495
21. Kopriva S, Koprivova A (2004) Plant adenosine 59-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55: 1775-1783
22. Koroleva OA, Davies A, Deeken R, Thorpe MR, Tomos AD, Hedrich R (2000) Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk. Plant Physiol 124: 599-608
23. Koroleva OA, Gibson TM, Cramer R, Stain C (2010) Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation. Plant J 64: 456-469
24. Krueger RJ, Siegel LM (1982) Spinach siroheme enzymes: isolation and characterization of ferredoxin-sulfite reductase and comparison of properties with ferredoxin-nitrite reductase. Biochemistry 21: 2892-2904
25. Lang C, Popko J, Wirtz M, Hell R, Herschbach C, Kreuzwieser J, Rennenberg H, Mendel RR, Hänsch R (2007) Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide. Plant Cell Environ 30: 447-455
26. Leustek T (2002) Sulfate metabolism. The Arabidopsis Book 1: e0017, doi/ 10.1199/tab.0017
27. Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120: 637-644
28. Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North KA, Kopriva S, Daniel-Vedele F (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39: 896-900
29. Nakamura M, Kuramata M, Kasugai I, Abe M, Youssefian S (2009) Increased thiol biosynthesis of transgenic poplar expressing a wheat O-acetylserine(thiol) lyase enhances resistance to hydrogen sulfide and sulfur dioxide toxicity. Plant Cell Rep 28: 313-323
30. Nakayama M, Akashi T, Hase T (2000) Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82: 27-32
31. Nandi PK, Agrawal M, Agrawal SB, Rao DN (1990) Physiological responses of Vicia faba plants to sulfur dioxide. Ecotoxicol Environ Saf 19: 64-71
32. Noji M, Saito M, Nakamura M, Aono M, Saji H, Saito K (2001) Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol 126: 973-980
33. 2. Plant Physiol 85: 928-933
34. 2exposure in Arabidopsis thaliana. Plant Cell Environ 35: 100-115
35. Ranieri A, Castagna A, Bini L, Soldatini GF (1995) Two-dimensional electrophoresis of thylakoid protein patterns in two wheat cultivars with different sensitivity to sulfur dioxide. Electrophoresis 16: 1301-1304
36. Ravilious GE, Jez JM (2012) Structural biology of plant sulfur metabolism: from assimilation to biosynthesis. Nat Prod Rep 29: 1138-1152
37. 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
38. Sekine K, Fujiwara M, Nakayama M, Takao T, Hase T, Sato N (2007) DNA binding and partial nucleoid localization of the chloroplast stromal enzyme ferredoxin:sulfite reductase. FEBS J 274: 2054-2069
39. Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277: 24399-24404
40. Sønderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates: gene discovery and beyond. Trends Plant Sci 15: 283-290
41. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641
42. Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 59-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32: 879-889 Van Der
43. Van Der Kooij TAW, De Kok LJ, Haneklaus S, Schnug E (1997) Uptake and metabolism of sulphur dioxide by Arabidopsis thaliana. New Phytol 135: 101-107
44. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krähenbühl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 59-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31: 729-740
45. Wang YH (2008) How effective is T-DNA insertional mutagenesis in Arabidopsis? Journal of Biochemical Technology 1: 11-20
46. Wen J-Q, Wen B-C, Wen H-G (1996) Changes in protein and amino acid levels during growth and senescence of Nicotiana rustica callus. J Plant Physiol 148: 707-710
47. 3at low concentrations in tobacco chloroplasts. Plant Cell Physiol 52: 1734-1743
48. 2as sulfur source for Chinese cabbage. J Plant Nutr Soil Sci 169: 529-534
49. Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122: 887-894
50. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 18: 131-146