Functional characterization of long-chain prenyl diphosphate synthases from tomato

Biochemical Journal

Volumn 449, Issue 3, 2013, Pages 729-740

  Jones, Matthew O ^a   Perez Fons, Laura ^a   Robertson, Francesca P ^a   Bramley, Peter M ^a   Fraser, Paul D ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Isoprenoid; Plastoquinone; Solanesol; Tomato; Ubiquinone; Virus induced gene silencing (VIGS)

Indexed keywords

DECAPRENYL DIPHOSPHATE; ISOPRENE; PLASTOQUINONE; PRENYL DIPHOSPHATE SYNTHASE; PYROPHOSPHATE; SOLANESYL; UBIQUINONE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CHLOROPLAST; CLONING; CONTROLLED STUDY; ELECTROSPRAY; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENE SILENCING; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLISM; NANO ELECTROSPRAY IONIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT LEAF; PLASTID; PRIORITY JOURNAL; PROTEIN PURIFICATION; THYLAKOID MEMBRANE; TOBACCO; TOMATO; TRANSMISSION ELECTRON MICROSCOPY;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; CLONING, MOLECULAR; DNA, PLANT; GENE SILENCING; GENES, PLANT; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLASTOQUINONE; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TERPENES;

ESCHERICHIA COLI; LYCOPERSICON; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

EID: 84872446517     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120988     Document Type: Article

References (49)

1. Doyle, M. P., Li, L. B., Yu, L. and Yu, C. A. (1989) Identification of a Mr = 17,000 protein as the plastoquinone-binding protein in the cytochrome b 6-f complex from spinach chloroplasts. J. Biol. Chem. 264, 1387-1392
2. Norris, S. R., Shen, X. and DellaPenna, D. (1998) Complementation of the Arabidopsis pds1 mutation with the gene encoding p-hydroxyphenylpyruvate dioxygenase. Plant Physiol. 117, 1317-1323 (Pubitemid 128652904)
3. Pfannschmidt, T., Bräutigam, T., Wagner, R., Dietzel, L., Schröter, Y., Steiner, S. and Nykytenko, A. (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann. Bot. 103, 599-607
4. Ernster, L., Lee, I. Y., Norling, B. and Persson, B. (1969) Studies with ubiquinone-depleted submitochondrial particles. Essentiality of ubiquinone for the interaction of succinate dehydrogenase, NADH dehydrogenase, and cytochrome b . Eur. J. Biochem. 9, 299-310
5. Rodríguez-Concepción, M. and Boronat, A. (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130, 1079-1089 (Pubitemid 35352936)
6. Disch, A., Hemmerlin, A., Bach, T. J. and Rohmer, M. (1998) Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. Biochem. J. 331, 615-621 (Pubitemid 28182180)
7. Fukusaki, E., Takeno, S., Bamba, T., Okumoto, H., Katto, H., Kajiyama, S. and Kobayashi, A. (2004) Biosynthetic pathway for the C45 polyprenol, solanesol, in tobacco. Biosci. Biotechnol. Biochem. 68, 1988-1990 (Pubitemid 39415270)
8. Okada, K., Suzuki, K., Kamiya, Y., Zhu, X., Fujisaki, S., Nishimura, Y., Nishino, T., Nakagawa, T., Kawamukai, M. and Matsuda, H. (1996) Polyprenyl diphosphate synthase essentially defines the length of the side chain of ubiquinone. Biochim. Biophys. Acta 1302, 217-223 (Pubitemid 26264554)
9. Ohnuma, S., Koyama, T. and Ogura, K. (1991) Purification of solanesyl-diphosphate synthase from Micrococcus luteus. A new class of prenyltransferase. J. Biol. Chem. 266, 23706-23713 (Pubitemid 21908855)
10. Sadre, R., Frentzen, M., Saeed, M. and Hawkes, T. (2010) Catalytic reactions of the homogentisate prenyl transferase involved in plastoquinone-9 biosynthesis. J. Biol. Chem. 285, 18191-18198
11. Cheng, Z., Sattler, S., Maeda, H., Sakuragi, Y., Bryant, D. A. and DellaPenna, D. (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15, 2343-2356 (Pubitemid 37261806)
12. Okada, K., Ohara, K., Yazaki, K., Nozaki, K., Uchida, N., Kawamukai, M., Nojiri, H. and Yamane, H. (2004) The AtPPT1 gene encoding 4-hydroxybenzoate polyprenyl diphosphate transferase in ubiquinone biosynthesis is required for embryo development in Arabidopsis thaliana. Plant Mol. Biol. 55, 567-577 (Pubitemid 40653985)
13. Yen, H. C., Shelton, B. A., Howard, L. R., Lee, S., Vrebalov, J. and Giovannoni, J. J. (1997) The tomato high-pigment (hp) locus maps to chromosome 2 and influences plastome copy number and fruit quality. Theor. Appl. Genet 95, 1069-1079 (Pubitemid 27526369)
14. Mustilli, A. C., Fenzi, F., Ciliento, R., Alfano, F. and Bowler, C. (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11, 145-157
15. Liu, Y., Roof, S., Zhibiao, Y., Barry, C., van Tuinen, A., Vrebalov, J., Bowler, C. and Giovannoni, J. (2008) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc. Natl. Acad. Sci. U.S.A. 101, 9897-9902 (Pubitemid 38869333)
16. Davuluri, G. R., van Tuinen, A., Fraser, P. D., Manfredonia, A., Newman, R., Burgess, D., Brummell, D. A., King, S. R., Palys, J., Uhlig, J. et al. (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat. Biotechnol. 23, 890-895 (Pubitemid 43093134)
17. Enfissi, E. M. A., Barneche, F., Ahmed, I., Lichtle, C., Gerrish, C., McQuinn, R. P., Giovannoni, J. J., Lopez-Juez, E., Bramley, P. M. and Fraser, P. D. (2010) Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22, 1190-1215
18. Karimi, M., Inzé, D. and Depicker, A. (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195 (Pubitemid 36725938)
19. Horsch, R. B., Fry, J. E., Hoffmann, N. L., Eichholtz, D., Rogers, S. G. and Fralet, R. T. (1985) A simple and general method for transferring genes into plants. Science 227, 1229-1231
20. Voinnet, O., Rivas, S., Mestre, P. and Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956 (Pubitemid 36339384)
21. Cho, H. and Winans, S. C. (2005) VirA and VirG activate the Ti plasmid repABC operon, elevating plasmid copy number in response to wound-released chemical signals. Proc. Natl. Acad. Sci. U.S.A. 102, 14843-14848 (Pubitemid 41457143)
22. Liu, Y., Schiff, M. and Dinesh-Kumar, S. P. (2002) Virus-induced gene silencing in tomato. Plant J. 31, 777-786
23. Schevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68, 850-858
24. Fraser, P. D., Pinto, M. E., Holloway, D. E. and Bramley, P. M. (2000) Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 24, 551-558
25. Phatthiya, A., Takahashi, S., Chareonthiphakorn, N., Koyama, T., Wititsuwannakul, D. and Wititsuwannakul, R. (2007) Cloning and expression of the gene encoding solanesyl diphosphate synthase from Hevea brasiliensis. Plant Sci. 172, 824-831
26. Fujii, H., Koyama, T. and Ogura, K. (1982) Efficient enzymatic hydrolysis of polyprenyl pyrophosphates. Biochim. Biophys. Acta 712, 716-718
27. Jayaraj, J. and Punja, Z. K. (2008) Transgenic carrot plants accumulating ketocarotenoids show tolerance to UV and oxidative stresses. Plant Physiol. Biochem. 46, 875-883
28. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M. and Rice-Evans, C. (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 26, 1231-1237 (Pubitemid 29262709)
29. Ohara, K., Sasaki, K. and Yazaki, K. (2010) Two solanesyl diphosphate synthases with different subcellular localizations and their respective physiological roles in Oryza sativa . J. Exp. Bot. 61, 2683-2692
30. Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016
31. Jun, L., Saiki, R., Tatsumi, K., Nakagawa, T. and Kawamukai, M. (2004) Identification and subcellular localization of two solanesyl diphosphate synthases from Arabidopsis thaliana . Plant Cell Physiol. 45, 1882-1888
32. Hirooka, K., Izumi, Y., An, C. I., Nakazawa, Y., Fukusaki, E. and Kobayashi, A. (2005) Functional analysis of two solanesyl diphosphate synthases from Arabidopsis thaliana . Biosci. Biotechnol. Biochem. 69, 592-601 (Pubitemid 40589120)
33. Hiooka, K., Bamba, T., Fukusaki, E. and Kobayashi, A. (2003) Cloning and kinetic characterization of Arabidopsis thaliana solanesyl diphosphate synthase. Biochem. J. 370, 679-686 (Pubitemid 36315156)
34. Ohara, K., Yamamoto, K., Hamamoto, M., Sasaki, K. and Yazaki, K. (2006) Functional characterization of OsPPT1, which encodes p-hydroxybenzoate polyprenyltransferase involved in ubiquinone biosynthesis in Oryza sativa . Plant Cell Physiol. 47, 581-590 (Pubitemid 43987604)
35. Ohnuma, S., Koyama, T. and Ogura, K. (1992) Chain length distribution of the products formed in solanesyl diphosphate synthase reaction. J. Biol. Chem. 112, 743-74
36. Melzer, M. and Heide, L. (1994) Characterization of polyphenyl diphosphate: 4-hydroxybenzoate polyprenyltransferase from Escherichia coli. Biochim. Biophys. Acta 1212, 93-102
37. Sadre, R., Gruber, J. and Frentzen, M. (2006) Characterization of homogentisate prenyltransferases involved in plastoquinone-9 and tocochromanol biosynthesis. FEBS Lett. 580, 5357-5362 (Pubitemid 44415814)
38. Hsieh, F.-L., Chang, T.-H., Ko, T.-P. and Wang, A. H.-J. (2011) Structure and mechanism of an Arabidopsis medium/long-chain-length prenyl pyrophosphate synthase. Plant Physiol. 155, 1079-1090
39. Ducluzeau, A.-L., Wamboldt, Y., Elowsky, C. G., Mackenzie, S. A., Schuurink, R. C. and Basset, G. J. C. (2011) Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. Plant J. 69, 366-375
40. Tian, L., DellaPenna, D. and Dixon, R. A. (2007) The pds2 mutation is a lesion in the Arabidopsis homogentisate solanesyl transferase gene involved in plastoquinone biosynthesis. Planta 226, 1067-1073 (Pubitemid 47283096)
41. Joyard, J., Ferro, M., Masselon, C., Seigneurin-Berny, D., Salvi, D., Garin, J. and Rolland, N. (2009) Chloroplast proteomics and the compartmentalisation of plastidial isoprenoid biosynthetic pathways. Mol. Plant 2, 1154-1180
42. Carol, P. and Kuntz, M. (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant. Sci. 6, 31-36 (Pubitemid 33141453)
43. Dalla Vecchia, F., Barbato, R., La Rocca, N., Moro, I. and Rascio, N. (2001) Responses to bleaching herbicides by leaf chloroplasts of maize plants grown at different temperatures. J. Exp. Bot. 52, 811-820 (Pubitemid 32623723)
44. Orzaez, D., Medina, A., Torre, S., Fernández-Moreno, J. P., Rambla, J. L., Fernández-del-Carmen, A., Butelli, E., Martin, C. and Granell, A. (2009) A visual reporter system for virus-induced gene silencing in tomato fruit based on anthocyanin accumulation. Plant Physiol. 150, 1122-1134
45. Misiti, D., Moore, H. W. and Folkers, K. (1965) Identification of plastoquinone-3 from chloroplasts. J. Am. Chem. Soc. 87, 1402-1403
46. Kruk, J., Schmid, G. H. and Strzalka, K. (1994) Antioxidant properties of plastoquinol and other biological prenylquinols in liposomes and solution. Free Radical Res. 21, 409-416 (Pubitemid 24349819)
47. Maciejewska, U., Polkowska-Kowalczyk, L., Swiezewska, E. and Szkopinska, A. (2002) Plastoquinone: possible involvement in plant disease resistance. Acta Biochim. Pol. 49, 775-780 (Pubitemid 135700602)
48. Bajda, A., Konopka-Postupolska, D., Krzymowska, M., Hennig, J., Skorupinska-Tude, K., Surmacz, L., Wojcik, J., Matysiak, Z., Chojnacki, T., Skorzynska-Polit, E. et al. (2009) Role of polyisoprenoids in tobacco resistance against biotic stresses. Physiol. Plant. 135, 351-364
49. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (Pubitemid 47236692)