Thioredoxin redox regulates ATpase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plant

Plant Physiology

Volumn 159, Issue 1, 2012, Pages 118-130

  Luo, Tao ^a,b   Fan, Tingting ^a   Liu, Yinan ^a   Rothbart, Maxi ^b   Yu, Jing ^a   Zhou, Shuaixiang ^a   Grimm, Bernhard ^b   Luo, Meizhong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PISUM SATIVUM;

EID: 84860551566     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.195446     Document Type: Article

References (67)

1. Adhikari ND, Froehlich JE, Strand DD, Buck SM, Kramer DM, Larkin RM (2011) GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23: 1449-1467
2. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustün S, Melzer M, Petersen K, Lein W, Börnke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22: 1498-1515
3. Balmer Y, Koller A, del Val G, Manieri W, Schürmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100: 370-375
4. Balmer Y, Stritt-Etter A-L, Hirasawa M, Jacquot J-P, Keryer E, Knaff DB, Schürmann P (2001) Oxidation-reduction and activation properties of chloroplast fructose 1,6-bisphosphatase with mutated regulatory site. Biochemistry 40: 15444-15450
5. Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60: 43-73
6. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220
7. Chi YH, Moon JC, Park JH, Kim H-S, Zulfugarov IS, Fanata WI, Jang HH, Lee JR, Lee YM, Kim ST, et al (2008) Abnormal chloroplast development and growth inhibition in rice thioredoxin m knock-down plants. Plant Physiol 148: 808-817
8. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin J-M, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747-23752
9. Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz K-J, Issakidis-Bourguet E (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136: 4088-4095
10. Constantin GD, Krath BN, MacFarlane SA, Nicolaisen M, Johansen IE, Lund OS (2004) Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant J 40: 622-631
11. Czarnecki O, Grimm B (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63: 1675-1687
12. Dai S, Friemann R, Glauser DA, Bourquin F, Manieri W, Schürmann P, Eklund H (2007) Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase. Nature 448: 92-96
13. Dai S, Schwendtmayer C, Johansson K, Ramaswamy S, Schürmann P, Eklund H (2000) How does light regulate chloroplast enzymes? Structure-function studies of the ferredoxin/thioredoxin system. Q Rev Biophys 33: 67-108
14. Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15: 1129-1159
15. Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155: 1477-1485
16. Fey V, Wagner R, Bräutigam K, Pfannschmidt T (2005) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56: 1491-1498
17. Gehl C, Waadt R, Kudla J, Mendel R-R, Hänsch R (2009) New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol Plant 2: 1051-1058
18. Gibson LC, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M, Hunter CN (1996) A putative Mg chelatase subunit from Arabidopsis thaliana cv C24: sequence and transcript analysis of the gene, import of the protein into chloroplasts, and in situ localization of the transcript and protein. Plant Physiol 111: 61-71
19. Gibson LC, Willows RD, Kannangara CG, von Wettstein D, Hunter CN (1995) Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli. Proc Natl Acad Sci USA 92: 1941-1944
20. Guo R, Luo M, Weinstein JD (1998) Magnesium-chelatase from developing pea leaves. Plant Physiol 116: 605-615
21. Hoffmann A, Hammes E, Plieth C, Desel C, Sattelmacher B, Hansen UP (2005) Effect of CO2 supply on formation of reactive oxygen species in Arabidopsis thaliana. Protoplasma 227: 3-9
22. Ikegami A, Yoshimura N, Motohashi K, Takahashi S, Romano PGN, Hisabori T, Takamiya K -i, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282: 19282-19291
23. Jacquot J-P, Lancelin J-M, Meyer Y (1997) Thioredoxins: structure and function in plant cells. New Phytol 136: 543-570
24. Jensen PE, Gibson LCD, Henningsen KW, Hunter CN (1996a) Expression of the chlI, chlD, and chlH genes from the Cyanobacterium synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity. J Biol Chem 271: 16662-16667
25. Jensen PE, Reid JD, Hunter CN (2000) Modification of cysteine residues in the ChlI and ChlH subunits of magnesium chelatase results in enzyme inactivation. Biochem J 352: 435-441
26. Jensen PE, Willows RD, Petersen BL, Vothknecht UC, Stummann BM, Kannangara CG, von Wettstein D, Henningsen KW (1996b) Structural genes for Mg-chelatase subunits in barley: Xantha-f, -g and -h. Mol Gen Genet 250: 383-394
27. Kirchsteiger K, Pulido P, González M, Cejudo FJ (2009) NADPH thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in Arabidopsis thaliana. Mol Plant 2: 298-307
28. Kobayashi T, Ito K (1999) Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J 18: 1192-1198
29. König J, Baier M, Horling F, Kahmann U, Harris G, Schürmann P, Dietz K-J (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 99: 5738-5743
30. Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902-906
31. Lepistö A, Kangasjärvi S, Luomala E-M, Brader G, Sipari N, Keränen M, Keinänen M, Rintamäki E (2009) Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 149: 1261-1276
32. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In RD Lester Packer, ed, Methods in Enzymology, Vol 148. Academic Press, Waltham, MA, pp 350-382
33. Luo M, Weinstein JD, Walker CJ (1999) Magnesium chelatase subunit D from pea: characterization of the cDNA, heterologous expression of an enzymatically active protein and immunoassay of the native protein. Plant Mol Biol 41: 721-731
34. Meyer Y, Siala W, Bashandy T, Riondet C, Vignols F, Reichheld JP (2008) Glutaredoxins and thioredoxins in plants. Biochim Biophys Acta 1783: 589-600
35. Miginiac-Maslow M, Lancelin J-M (2002) Intrasteric inhibition in redox signalling: light activation of NADP-malate dehydrogenase. Photosynth Res 72: 1-12
36. Miller M, Schürmann P, Hodges M, Jacquot J-P (2004) Isolation of pea thioredoxin f precursor protein and characterization of its biochemical properties. Photosynth Res 79: 287-294
37. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053-2058
38. Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33: 737-742
39. Nott A, Jung H-S, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739-759
40. Papenbrock J, Mishra S, Mock H-P, Kruse E, Schmidt E-K, Petersmann A, Braun H-P, Grimm B (2001) Impaired expression of the plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic phenotype of transformed tobacco plants. Plant J 28: 41-50
41. Papenbrock J, Mock H-P, Tanaka R, Kruse E, Grimm B (2000a) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122: 1161-1169
42. Papenbrock J, Pfündel E, Mock H-P, Grimm B (2000b) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J 22: 155-164
43. Peter E, Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2: 1198-1210
44. Petersen BL, Jensen PE, Gibson LC, Stummann BM, Hunter CN, Henningsen KW (1998) Reconstitution of an active magnesium chelatase enzyme complex from the bchI, -D, and -H gene products of the green sulfur bacterium Chlorobium vibrioforme expressed in Escherichia coli. J Bacteriol 180: 699-704
45. Pfannschmidt T, Allen JF, Oelmüller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112: 1-9
46. Pontier D, Albrieux C, Joyard J, Lagrange T, Block MA (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis: effects on chloroplast development and on chloroplast-to-nucleus signaling. J Biol Chem 282: 2297-2304
47. Pulido P, Spínola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz K-J, González M, Cejudo FJ (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J Exp Bot 61: 4043-4054
48. Richter A, Peter E, Pörs Y, Lorenzen S, Grimm B, Czarnecki O (2010) Rapid dark repression of 5-aminolevulinic acid synthesis in green barley leaves. Plant Cell Physiol 51: 670-681
49. Ruckle ME, DeMarco SM, Larkin RM (2007) Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19: 3944-3960
50. Samra HS, Gao F, He F, Hoang E, Chen Z, Gegenheimer PA, Berrie CL, Richter ML (2006) Structural analysis of the regulatory dithiol-containing domain of the chloroplast ATP synthase g subunit. J Biol Chem 281: 31041-31049
51. Sawers RJ, Viney J, Farmer PR, Bussey RR, Olsefski G, Anufrikova K, Hunter CN, Brutnell TP (2006) The maize Oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Mol Biol 60: 95-106
52. Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10: 1235-1274
53. Shang Y, Yan L, Liu Z-Q, Cao Z, Mei C, Xin Q, Wu F-Q, Wang X-F, Du S-Y, Jiang T, et al (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22: 1909-1935
54. Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y, et al (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443: 823-826
55. Sparla F, Pupillo P, Trost P (2002) The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem 277: 44946-44952
56. Stenbaek A, Hansson A, Wulff RP, Hansson M, Dietz K-J, Jensen PE (2008) NADPH-dependent thioredoxin reductase and 2-Cys peroxiredoxins are needed for the protection of Mg-protoporphyrin monomethyl ester cyclase. FEBS Lett 582: 2773-2778
57. Stenbaek A, Jensen PE (2010) Redox regulation of chlorophyll biosynthesis. Phytochemistry 71: 853-859
58. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321-346
59. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194
60. Tovar-Méndez A, Matamoros MA, Bustos-Sanmamed P, Dietz KJ, Cejudo FJ, Rouhier N, Sato S, Tabata S, Becana M (2011) Peroxiredoxins and NADPH-dependent thioredoxin systems in the model legume Lotus japonicus. Plant Physiol 156: 1535-1547
61. Tsuzuki T, Takahashi K, Inoue S, Okigaki Y, Tomiyama M, Hossain MA, Shimazaki K, Murata Y, Kinoshita T (2011) Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J Plant Res 124: 527-538
62. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, et al (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306: 1183-1185
63. Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571: 119-123
64. Wu F-Q, Xin Q, Cao Z, Liu Z-Q, Du S-Y, Mei C, Zhao C-X, Wang X-F, Shang Y, Jiang T, et al (2009) The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol 150: 1940-1954
65. Zhang H, Li J, Yoo J-H, Yoo S-C, Cho S-H, Koh H-J, Seo HS, Paek N-C (2006) Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62: 325-337
66. Zhang N, Portis AR Jr (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96: 9438-9443
67. Zhou S, Sawicki A, Willows RD, Luo M (2012) C-terminal residues of oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis. FEBS Lett 586: 205-210