Structure and mechanism of an arabidopsis medium/long-chain-length prenyl pyrophosphate synthase

Plant Physiology

Volumn 155, Issue 3, 2011, Pages 1079-1090

  Hsieh, Fu Lien ^a,c,d   Chang, Tao Hsin ^a,d   Ko, Tzu Ping ^a,b   Wang, Andrew H J ^a,b,c  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79952291036     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.168799     Document Type: Article

References (69)

1. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FW, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15: 2866-2884
2. Artz JD, Dunford JE, Arrowood MJ, Dong A, Chruszcz M, Kavanagh KL, Minor W, Russell RG, Ebetino FH, Oppermann U, et al (2008) Targeting a uniquely nonspecific prenyl synthase with bisphosphonates to combat cryptosporidiosis. Chem Biol 15: 1296-1306
3. Bouvier F, Suire C, d'Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24: 241-252
4. Brünger AT (1993) Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr D Biol Crystallogr 49: 24-36
5. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, et al (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921
6. Burke C, Croteau R (2002) Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch Biochem Biophys 405: 130-136
7. Burke CC, Wildung MR, Croteau R (1999) Geranyl diphosphate synthase: cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc Natl Acad Sci USA 96: 13062-13067
8. Cervantes-Cervantes M, Gallagher CE, Zhu C, Wurtzel ET (2006) Maize cDNAs expressed in endosperm encode functional farnesyl diphosphate synthase with geranylgeranyl diphosphate synthase activity. Plant Physiol 141: 220-231
9. Chang TH, Guo RT, Ko TP, Wang AH, Liang PH(2006) Crystal structure of type-III geranylgeranyl pyrophosphate synthase from Saccharomyces cerevisiae and the mechanism of product chain length determination. J Biol Chem 281: 14991-15000
10. Chang TH, Hsieh FL, Ko TP, Teng KH, Liang PH, Wang AH (2010) Structure of a heterotetrameric geranyl pyrophosphate synthase from mint (Mentha piperita) reveals intersubunit regulation. Plant Cell 22: 454-467
11. Chen A, Poulter CD (1993) Purification and characterization of farnesyl diphosphate/geranylgeranyl diphosphate synthase: a thermostable bifunctional enzyme from Methanobacterium thermoautotrophicum. J Biol Chem 268: 11002-11007
12. Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15: 481-494
13. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) MolProbity: allatom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21
14. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011
15. Davis AR, Pylatuik JD, Paradis JC, Low NH (1998) Nectar-carbohydrate production and composition vary in relation to nectary anatomy and location within individual flowers of several species of Brassicaceae. Planta 205: 305-318
16. DeLano WL (2002) The PyMOL Molecular Graphic System. DeLano Scientific, Palo Alto, CA
17. Derewenda ZS (2004) Rational protein crystallization by mutational surface engineering. Structure 12: 529-535
18. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122: 627-633
19. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132
20. Engprasert S, Taura F, Kawamukai M, Shoyama Y (2004) Molecular cloning and functional expression of geranylgeranyl pyrophosphate synthase from Coleus forskohlii Briq. BMC Plant Biol 4: 1-18
21. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414
22. Goldschmidt L, Cooper DR, Derewenda ZS, Eisenberg D (2007) Toward rational protein crystallization: a Web server for the design of crystallizable protein variants. Protein Sci 16: 1569-1576
23. Guo RT, Kuo CJ, Chou CC, Ko TP, Shr HL, Liang PH, Wang AH (2004) Crystal structure of octaprenyl pyrophosphate synthase from hyperthermophilic Thermotoga maritima and mechanism of product chain length determination. J Biol Chem 279: 4903-4912
24. Hirooka K, Bamba T, Fukusaki E, Kobayashi A (2003) Cloning and kinetic characterization of Arabidopsis thaliana solanesyl diphosphate synthase. Biochem J 370: 679-686
25. Hosfield DJ, Zhang Y, Dougan DR, Broun A, Tari LW, Swanson RV, Finn J (2004) Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis. J Biol Chem 279: 8526-8529
26. Hsiao YY, Jeng MF, Tsai WC, Chuang YC, Li CY, Wu TS, Kuoh CS, Chen WH, Chen HH (2008) A novel homodimeric geranyl diphosphate synthase from the orchid Phalaenopsis bellina lacking a DD(X)2-4D motif. Plant J 55: 719-733
27. Hsieh FL, Chang TH, Ko TP, Wang AH (2010) Enhanced specificity of mint geranyl pyrophosphate synthase by modifying the R-loop interactions. J Mol Biol 404: 859-873
28. Jones ME (1971) The population genetics of Arabidopsis thaliana. I. The breeding system. Heredity 27: 39-50
29. Jun L, Saiki R, Tatsumi K, Nakagawa T, Kawamukai M (2004) Identification and subcellular localization of two solanesyl diphosphate synthases from Arabidopsis thaliana. Plant Cell Physiol 45: 1882-1888
30. Kainou T, Kawamura K, Tanaka K, Matsuda H, Kawamukai M (1999) Identification of the GGPS1 genes encoding geranylgeranyl diphosphate synthases from mouse and human. Biochim Biophys Acta 1437: 333-340
31. Kavanagh KL, Guo K, Dunford JE, Wu X, Knapp S, Ebetino FH, Rogers MJ, Russell RG, Oppermann U (2006) The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proc Natl Acad Sci USA 103: 7829-7834
32. Keegan RM, Winn MD (2008) MrBUMP: an automated pipeline for molecular replacement. Acta Crystallogr D Biol Crystallogr 64: 119-124
33. Kellogg BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1: 570-578
34. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144
35. Kirby J, Keasling JD (2009) Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol 60: 335-355
36. Kleywegt GJ (2007) Crystallographic refinement of ligand complexes. Acta Crystallogr D Biol Crystallogr 63: 94-100
37. Kloer DP, Welsch R, Beyer P, Schulz GE (2006) Structure and reaction geometry of geranylgeranyl diphosphate synthase from Sinapis alba. Biochemistry 45: 15197-15204
38. Lange BM, Ghassemian M (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol Biol 51: 925-948
39. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283-291
40. Lebedev AA, Vagin AA, Murshudov GN (2008) Model preparation in MOLREP and examples of model improvement using x-ray data. Acta Crystallogr D Biol Crystallogr 64: 33-39
41. Liang PH (2009) Reaction kinetics, catalytic mechanisms, conformational changes, and inhibitor design for prenyltransferases. Biochemistry 48: 6562-6570
42. Liang PH, Ko TP, Wang AH (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269: 3339-3354
43. Ling Y, Li ZH, Miranda K, Oldfield E, Moreno SN (2007) The farnesyldiphosphate/ geranylgeranyl-diphosphate synthase of Toxoplasma gondii is a bifunctional enzyme and a molecular target of bisphosphonates. J Biol Chem 282: 30804-30816
44. Lucast LJ, Batey RT, Doudna JA (2001) Large-scale purification of a stable form of recombinant tobacco etch virus protease. Biotechniques 30: 544-546, 548, 550
45. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41
46. Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172: 6704-6712
47. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
48. Ogura K, Koyama T (1998) Enzymatic aspects of isoprenoid chain elongation. Chem Rev 98: 1263-1276
49. Ohnuma S, Hirooka K, Hemmi H, Ishida C, Ohto C, Nishino T (1996) Conversion of product specificity of archaebacterial geranylgeranyldiphosphate synthase: identification of essential amino acid residues for chain length determination of prenyltransferase reaction. J Biol Chem 271: 18831-18837
50. Orlova I, Nagegowda DA, Kish CM, Gutensohn M, Maeda H, Varbanova M, Fridman E, Yamaguchi S, Hanada A, Kamiya Y, et al (2009) The small subunit of snapdragon geranyl diphosphate synthase modifies the chain length specificity of tobacco geranylgeranyl diphosphate synthase in planta. Plant Cell 21: 4002-4017
51. Otwinowski Z, Minor W (1997) Processing of x-ray diffraction data collected in oscillation mode. Macromolecular Crystallography 276: 307-326
52. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science 311: 808-811
53. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425
54. Schmidt A, Gershenzon J (2008) Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69: 49-57
55. Schmidt A, Wächtler B, Temp U, Krekling T, Séguin A, Gershenzon J (2010) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Picea abies. Plant Physiol 152: 639-655
56. Schwarzenbacher R, Godzik A, Grzechnik SK, Jaroszewski L (2004) The importance of alignment accuracy for molecular replacement. Acta Crystallogr D Biol Crystallogr 60: 1229-1236
57. Snape JW, Lawrence MJ (1971) Breeding system of Arabidopsis thaliana. Heredity 27: 299-301
58. Soll J, Schultz G, Joyard J, Douce R, Block MA (1985) Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Arch Biochem Biophys 238: 290-299
59. Sun HY, Ko TP, Kuo CJ, Guo RT, Chou CC, Liang PH, Wang AH (2005) Homodimeric hexaprenyl pyrophosphate synthase from the thermoacidophilic crenarchaeon Sulfolobus solfataricus displays asymmetric subunit structures. J Bacteriol 187: 8137-8148
60. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599
61. Tarshis LC, Proteau PJ, Kellogg BA, Sacchettini JC, Poulter CD (1996) Regulation of product chain length by isoprenyl diphosphate synthases. Proc Natl Acad Sci USA 93: 15018-15023
62. Tholl D, Kish CM, Orlova I, Sherman D, Gershenzon J, Pichersky E, Dudareva N (2004) Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16: 977-992
63. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
64. Vandermoten S, Charloteaux B, Santini S, Sen SE, Béliveau C, Vandenbol M, Francis F, Brasseur R, Cusson M, Haubruge E (2008) Characterization of a novel aphid prenyltransferase displaying dual geranyl/ farnesyl diphosphate synthase activity. FEBS Lett 582: 1928-1934
65. Van Schie CC, Ament K, Schmidt A, Lange T, Haring MA, Schuurink RC (2007) Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J 52: 752-762
66. Wang G, Dixon RA (2009) Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc Natl Acad Sci USA 106: 9914-9919
67. Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24: 1441-1447
68. Ye Y, Fujii M, Hirata A, Kawamukai M, Shimoda C, Nakamura T (2007) Geranylgeranyl diphosphate synthase in fission yeast is a heteromer of farnesyl diphosphate synthase (FPS), Fps1, and an FPS-like protein, Spo9, essential for sporulation. Mol Biol Cell 18: 3568-3581
69. Zhu XF, Suzuki K, Okada K, Tanaka K, Nakagawa T, Kawamukai M, Matsuda K (1997) Cloning and functional expression of a novel geranylgeranyl pyrophosphate synthase gene from Arabidopsis thaliana in Escherichia coli. Plant Cell Physiol 38: 357-361