ATR3 encodes a diflavin reductase essential for Arabidopsis embryo development

New Phytologist

Volumn 187, Issue 1, 2010, Pages 67-82

  Varadarajan, Janani ^a   Guilleminot, Jocelyne ^b   Saint Jore Dupas, Claude ^c   Piégu, Benoît ^b   Chabouté, Marie Edith ^d   Gomord, Véronique ^c   Coolbaugh, Ronald C ^a   Devic, Martine ^b   Delorme, Valérie ^b  

^a PURDUE UNIVERSITY   (United States)

^b CNRS   (France)

^c UNIVERSITÉ DE ROUEN   (France)

^d INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

CIAPIN1; Cytochrome P450 reductase (CPR); Dre2; Embryogenesis; FRE 1; NR1; TAH18

Indexed keywords

ARABIDOPSIS PROTEIN; ATR3 PROTEIN, ARABIDOPSIS; CIAPIN1 PROTEIN, HUMAN; CYP1A2 PROTEIN, HUMAN; CYTOCHROME C; CYTOCHROME P450 1A2; OXIDOREDUCTASE; SIGNAL PEPTIDE; PROTEIN BINDING;

APOPTOSIS; CYTOCHROME; CYTOLOGY; DICOTYLEDON; EMBRYONIC DEVELOPMENT; ENZYME ACTIVITY; PHYLOGENETICS; PHYTOCHEMISTRY; YEAST;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL CYCLE; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; EMBRYO DEVELOPMENT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PLANT SEED; PRENATAL DEVELOPMENT; PROTEIN BINDING; PROTEIN TRANSPORT; EMBRYOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE; CELL NUCLEUS; CYTOCHROME P-450 CYP1A2; CYTOCHROMES C; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES; PROTEIN BINDING; PROTEIN TRANSPORT; SEEDS;

ANIMALIA; ARABIDOPSIS;

EID: 77954575964     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03254.x     Document Type: Article

References (61)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997, 25:3389-3402.
3. Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M. Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Molecular and Cellular Biology 1997, 17:3094-3102.
4. Barroco RM, Van Poucke K, Bergervoet JH, De Veylder L, Groot SP, Inze D, Engler G. The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiology 2005, 137:127-140.
5. Bechtold N, Ellis J, Pelletier G. In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Comptes Rendus. Académie des Sciences 1993, 316:1194-1199.
6. Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, Hieter P. Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Molecular Cell 2008, 30:248-258.
7. Blazquez MA, Soowal LN, Lee I, Weigel D. LEAFY expression and flower initiation in Arabidopsis. Development 1997, 124:3835-3844.
8. Bowman J. Arabidopsis, an atlas of morphology and development 1994, New York, NY, USA, Springer-Verlag
9. Bozhkov PV, Filonova LH, Suarez MF. Programmed cell death in plant embryogenesis. Current Topics in Developmental Biology 2005, 67:135-179.
10. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 1991, 351:714-718.
11. Chaboute ME, Clement B, Philipps G. S phase and meristem-specific expression of the tobacco RNR1b gene is mediated by an E2F element located in the 5′ leader sequence. Journal of Biological Chemistry 2002, 277:17845-17851.
12. Chaboute ME, Clement B, Sekine M, Philipps G, Chaubet-Gigot N. Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell 2000, 12:1987-2000.
13. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 1998, 16:735-743.
14. Devic M, Albert S, Delseny M, Roscoe T. Efficient PCR walking on plant genomic DNA. Plant Physiology and Biochemistry 1997, 35:331-339.
15. Dignam JD, Strobel HW. Preparation of homogeneous NADPH-cytochrome P-450 reductase from rat liver. Biochemical and Biophysical Research Communications 1975, 63:845-852.
16. Finn RD, Basran J, Roitel O, Wolf CR, Munro AW, Paine MJ, Scrutton NS. Determination of the redox potentials and electron transfer properties of the FAD- and FMN-binding domains of the human oxidoreductase NR1. European Journal of Biochemistry 2003, 270:1164-1175.
17. Galtier N, Gouy M, Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 1996, 12:543-548.
18. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 2003, 52:696-704.
19. Hao Z, Li X, Qiao T, Fan D. Successful expression and purification of human CIAPIN1 in baculovirus-insect cell system and application of this system to investigation of its potential methyltransferase activity. International Journal of Biological Macromolecules 2008, 42:27-32.
20. Hao Z, Li X, Qiao T, Li S, Lv Y, Fan D. Downregulated expression of CIAPIN1 may contribute to gastric carcinogenesis by accelerating cell proliferation and promoting cell cycle progression. Cancer Biology & Therapy 2009, 8:1064-1070.
21. Huang N, Pandey AV, Agrawal V, Reardon W, Lapunzina PD, Mowat D, Jabs EW, Van Vliet G, Sack J, Fluck CE. Diversity and function of mutations in p450 oxidoreductase in patients with Antley-Bixler syndrome and disordered steroidogenesis. American Journal of Human Genetics 2005, 76:729-749.
22. Jenik PD, Jurkuta RE, Barton MK. Interactions between the cell cycle and embryonic patterning in Arabidopsis uncovered by a mutation in DNA polymerase epsilon. Plant Cell 2005, 17:3362-3377.
23. Karimi M, Inze D, Depicker A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 2002, 7:193-195.
24. Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K. Abolition of the tapetum suicide program ruins microsporogenesis. Plant and Cell Physiology 2006, 47:784-787.
25. Kwasnicka DA, Krakowiak A, Thacker C, Brenner C, Vincent SR. Coordinate expression of NADPH-dependent flavin reductase, Fre-1, and Hint-related 7meGMP-directed hydrolase, DCS-1. Journal of Biological Chemistry 2003, 278:39051-39058.
26. Leclerc D, Wilson A, Dumas R, Gafuik C, Song D, Watkins D, Heng HH, Rommens JM, Scherer SW, Rosenblatt DS. Cloning and mapping of a cDNA for methionine synthase reductase, a flavoprotein defective in patients with homocystinuria. Proceedings of the National Academy of Sciences, USA 1998, 95:3059-3064.
27. Li X, Pan Y, Fan R, Jin H, Han S, Liu J, Wu K, Fan D. Adenovirus-delivered CIAPIN1 small interfering RNA inhibits HCC growth in vitro and in vivo. Carcinogenesis 2008, 29:1587-1593.
28. Lin Z, Yin K, Zhu D, Chen Z, Gu H, Qu LJ. AtCDC5 regulates the G2 to M transition of the cell cycle and is critical for the function of Arabidopsis shoot apical meristem. Cell Research 2007, 17:815-828.
29. Liu H, Rodgers ND, Jiao X, Kiledjian M. The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO Journal 2002, 21:4699-4708.
30. Louerat-Oriou B, Perret A, Pompon D. Differential redox and electron-transfer properties of purified yeast, plant and human NADPH-cytochrome P-450 reductases highly modulate cytochrome P-450 activities. European Journal of Biochemistry 1998, 258:1040-1049.
31. Mankin SL, Allen CG, Thompson WF. Introduction of a plant intron into the luciferase gene of Photinus pyralis. Molecular Biology Reports 1997, 15:186-196.
32. Mayer U, Jurgens G. Pattern formation in plant embryogenesis: a reassessment. Seminars in Cell & Developmental Biology 1998, 9:187-193.
33. Mizutani M, Ohta D. Two isoforms of NADPH:cytochrome P450 reductase in Arabidopsis thaliana. Gene structure, heterologous expression in insect cells, and differential regulation. Plant Physiology 1998, 116:357-367.
34. Murataliev MB, Feyereisen R, Walker FA. Electron transfer by diflavin reductases. Biochimica et Biophysica Acta 2004, 1698:1-26.
35. Nagata T, Nemoto Y, Hasezawa S. Tobacco BY-2 cell line as the "Hela" cell in the cell biology of higher plants. International Review of Cytology 1992, 132:1-30.
36. Olteanu H, Banerjee R. Human methionine synthase reductase, a soluble P-450 reductase-like dual flavoprotein, is sufficient for NADPH-dependent methionine synthase activation. Journal of Biological Chemistry 2001, 276:35558-35563.
37. Ostrowski J, Barber MJ, Rueger DC, Miller BE, Siegel LM, Kredich NM. Characterization of the flavoprotein moieties of NADPH-sulfite reductase from Salmonella typhimurium and Escherichia coli. Physicochemical and catalytic properties, amino acid sequence deduced from DNA sequence of cysJ, and comparison with NADPH-cytochrome P-450 reductase. Journal of Biological Chemistry 1989, 264:15796-15808.
38. Paine MJ, Garner AP, Powell D, Sibbald J, Sales M, Pratt N, Smith T, Tew DG, Wolf CR. Cloning and characterization of a novel human dual flavin reductase. Journal of Biological Chemistry 2000, 275:1471-1478.
39. Paquette SM, Jensen K, Bak S. A web-based resource for the Arabidopsis P450, cytochromes b(5), NADPH-cytochrome P450 reductases, and family 1 glycosyltransferases (http://www.P450.kvl.dk). Phytochemistry 2009, 70(17-18):1940-1947.
40. Rappleye CA, Tagawa A, Le Bot N, Ahringer J, Aroian RV. Involvement of fatty acid pathways and cortical interaction of the pronuclear complex in Caenorhabditis elegans embryonic polarity. BMC Developmental Biology 2003, 3:8.
41. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends in Genetics 2000, 16:276-277.
42. Ro DK, Ehlting J, Douglas CJ. Cloning, functional expression, and subcellular localization of multiple NADPH-cytochrome P450 reductases from hybrid poplar. Plant Physiology 2002, 130:1837-1851.
43. Ronceret A, Gadea-Vacas J, Guilleminot J, Lincker F, Delorme V, Lahmy S, Pelletier G, Chaboute ME, Devic M. The first zygotic division in Arabidopsis requires de novo transcription of thymidylate kinase. Plant Journal 2008, 53:776-789.
44. Ronceret A, Guilleminot J, Lincker F, Gadea-Vacas J, Delorme V, Bechtold N, Pelletier G, Delseny M, Chaboute ME, Devic M. Genetic analysis of two Arabidopsis DNA polymerase epsilon subunits during early embryogenesis. Plant Journal 2005, 44:223-236.
45. Saint-Jore CM, Evins J, Batoko H, Brandizzi F, Moore I, Hawes C. Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant Journal 2002, 29:661-678.
46. Schmidt HH, Smith RM, Nakane M, Murad F. Ca2+/calmodulin-dependent NO synthase type I: a biopteroflavoprotein with Ca2+/calmodulin-independent diaphorase and reductase activities. Biochemistry 1992, 31:3243-3249.
47. Shen AL, O'Leary KA, Kasper CB. Association of multiple developmental defects and embryonic lethality with loss of microsomal NADPH-cytochrome P450 oxidoreductase. Journal of Biological Chemistry 2002, 277:6536-6541.
48. Shen AL, Sem DS, Kasper CB. Mechanistic studies on the reductive half-reaction of NADPH-cytochrome P450 oxidoreductase. Journal of Biological Chemistry 1999, 274:5391-5398.
49. Shibayama H, Takai E, Matsumura I, Kouno M, Morii E, Kitamura Y, Takeda J, Kanakura Y. Identification of a cytokine-induced antiapoptotic molecule anamorsin essential for definitive hematopoiesis. Journal of Experimental Medicine 2004, 199:581-592.
50. Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B, Kuttner F, Lepiniec L, Stierhof YD, Schwarz H. The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes and Development 2002, 16:959-971.
51. Tzafrir I, McElver JA, Liu Cm CM, Yang LJ, Wu JQ, Martinez A, Patton DA, Meinke DW. Diversity of TITAN functions in Arabidopsis seed development. Plant Physiology 2002, 128:38-51.
52. Urban P, Mignotte C, Kazmaier M, Delorme F, Pompon D. Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. Journal of Biological Chemistry 1997, 272:19176-19186.
53. Vernis L, Facca C, Delagoutte E, Soler N, Chanet R, Guiard B, Faye G, Baldacci G. A newly identified essential complex, Dre2-Tah18, controls mitochondria integrity and cell death after oxidative stress in yeast. PLoS ONE 2009, 4:e4376.
54. Wallace IM, O'Sullivan O, Higgins DG, Notredame C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Research 2006, 34:1692-1699.
55. Wang C, Liu Z. Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plant development. Plant Cell 2006, 18:350-365.
56. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS, Kim JJ. Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proceedings of the National Academy of Sciences, USA 1997, 94:8411-8416.
57. Werck-Reichhart D, Bak S, Paquette S. Cytochromes P450 2002, Rockville, MD, USA, American Society of Plant Biologists
58. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution 2001, 18:691-699.
59. Wroblewski T, Tomczak A, Michelmore R. Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnology Journal 2005, 3:259-273.
60. Yamazaki H, Shimada T. Cytochrome P450 reconstitution systems. Methods Mol Biol. 2006, 320:61-71.
61. Yasukochi Y, Masters BS. Some properties of a detergent-solubilized NADPH-cytochrome c (cytochrome P-450) reductase purified by biospecific affinity chromatography. Journal of Biological Chemistry 1976, 251:5337-5344.