Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis

Plant Journal

Volumn 69, Issue 2, 2012, Pages 366-375

  Ducluzeau, Anne Lise ^a   Wamboldt, Yashitola ^a   Elowsky, Christian G ^a   MacKenzie, Sally A ^a   Schuurink, Robert C ^b   Basset, Gilles J C ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Arabidopsis; isoprenoid; mitochondria; prenyl diphosphate synthase; ubiquinone

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS GENE; BENZOQUINONES; COENZYME Q; COMPLEMENTATION; DIPHOSPHATES; ELECTRON CARRIER; FUNCTIONAL NETWORK; FUSION EXPERIMENTS; GENE NETWORKS; GREEN FLUORESCENT PROTEIN; ISOPRENOIDS; ORTHOLOGS; OVER-EXPRESSION; PHYLOGENETIC ANALYSIS; PLASTOQUINONE; PRODUCT SPECIFICITY; REDOX-ACTIVE; SIDE-CHAINS; SOLANESYL DIPHOSPHATE; SYNTHASES; UBIQUINONE; WILD-TYPE PLANTS;

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; GENES; MITOCHONDRIA; REDOX REACTIONS;

PLANTS (BOTANY);

GREEN FLUORESCENT PROTEIN; OCTAPRENYLTRANSFERASE; PLASTOQUINONE; TERPENE; TRANS-OCTAPRENYLTRANSTRANSFERASE; TRANSFERASE; UBIQUINONE; UBIQUINONE 9;

ARABIDOPSIS; ARTICLE; CHEMISTRY; CHLOROPLAST; ENZYMOLOGY; GENE INACTIVATION; GENE REGULATORY NETWORK; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MITOCHONDRION; MOLECULAR CLONING; MUTATION; PHYLOGENY; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; TRANSGENIC PLANT; ULTRASTRUCTURE;

ALKYL AND ARYL TRANSFERASES; ARABIDOPSIS; CHLOROPLASTS; CLONING, MOLECULAR; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; MITOCHONDRIA; MUTATION; PHYLOGENY; PLANTS, GENETICALLY MODIFIED; PLASTOQUINONE; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; TERPENES; UBIQUINONE;

ARABIDOPSIS; EUKARYOTA; NICOTIANA TABACUM;

EID: 84855672979     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04796.x     Document Type: Article

References (34)

1. Ashby, M.N., and, Edwards, P.A., (1990) Elucidation of the deficiency in two yeast coenzyme Q mutants. Characterization of the structural gene encoding hexaprenyl pyrophosphate synthetase. J. Biol. Chem. 265, 13157-13164.
2. Avelange-Macherel, M.H., and, Joyard, J., (1998) Cloning and functional expression of AtCOQ3, the Arabidopsis homologue of the yeast COQ3 gene, encoding a methyltransferase from plant mitochondria involved in ubiquinone biosynthesis. Plant J. 14, 203-213. (Pubitemid 28236011)
3. Block, A., Guo, M., Li, G., Elowsky, C., Clemente, T.E., and, Alfano, J.R., (2010) The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell Microbiol. 12, 318-330.
4. Bouvier, F., Suire, C., d'Harlingue, A., Backhaus, R.A., and, Camara, B., (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J. 24, 241-252.
5. Christensen, A.C., Lyznik, A., Mohammed, S., Elowsky, C.G., Elo, A., Yule, R., and, Mackenzie, S.A., (2005) Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell, 17, 2805-2816.
6. Clarke, C.F., (2000) New advances in coenzyme Q biosynthesis. Protoplasma, 213, 134-147.
7. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. Dawson, R.M.C., Elliot, D.C., Elliot, W.H., and, Jones, K.M., (1986) Data for Biochemical Research. New York: Oxford University Press.
9. 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. 15, 615-621. (Pubitemid 28182180)
10. Gin, P., and, Clarke, C.F., (2005) Genetic evidence for a multi-subunit complex in coenzyme Q biosynthesis in yeast and the role of the Coq1 hexaprenyl diphosphate synthase. J. Biol. Chem. 280, 2676-2681. (Pubitemid 40189372)
11. Hirooka, 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)
12. 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.
13. Joyard, J., Ferro, M., Masselon, C., Seigneurin-Berny, D., Salvi, D., Garin, J., and, Rolland, N., (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol. Plant, 2, 1154-1180.
14. 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.
15. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
16. Kawamukai, M., (2009) Biosynthesis and bioproduction of coenzyme Q10 by yeasts and other organisms. Biotechnol. Appl. Biochem. 53, 217-226.
17. Kubo, H., Fujii, K., Kawabe, T., Matsumoto, S., Kishida, H., and, Hosoe, K., (2008) Food content of ubiquinol-10 and ubiquinone-10 in the Japanese diet. J. Food Compost. Anal. 21, 199-210.
18. Lange, B.M., and, Ghassemian, M., (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol. Biol. 51, 925-948. (Pubitemid 36579709)
19. Lenaz, G., and, Genova, M.L., (2009) Mobility and function of coenzyme Q (ubiquinone) in the mitochondrial respiratory chain. Biochim. Biophys. Acta 1787, 563-573.
20. Mackenzie, S.A., (2005) Plant organellar protein targeting: a traffic plan still under construction. Trends Cell Biol. 10, 548-554.
21. Nowicka, B., and, Kruk, J., (2010) Occurrence, biosynthesis and function of isoprenoid quinones. Biochim. Biophys. Acta 1797, 1587-1605.
22. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and, Kinoshita, K., (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987-D991.
23. 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)
24. 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.
25. 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)
26. Peeters, N., and, Small, I., (2001) Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta. 1541, 54-63. (Pubitemid 34024828)
27. Runquist, M., Ericsson, J., Thelin, A., Chojnacki, T., and, Dallner, G., (1994) Isoprenoid biosynthesis in rat liver mitochondria. Studies on farnesyl pyrophosphate synthase and trans-prenyltransferase. J. Biol. Chem. 269, 5804-5809.
28. van Schie, C.C., Ament, K., Schmidt, A., Lange, T., Haring, M.A., and, Schuurink, R.C., (2007) Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J. 52, 752-762. (Pubitemid 350060597)
29. Stowell, M.H., McPhillips, T.M., Rees, D.C., Soltis, S.M., Abresch, E., and, Feher, G., (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science, 276, 812-816. (Pubitemid 27199864)
30. Swiezewska, E., Dallner, G., Andersson, B., and, Ernster, L., (1993) Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. J. Biol. Chem. 268, 494-1499.
31. Whistance, G.R., Dillon, J.F., and, Threlfall, D.R., (1969) The nature, intergeneric distribution and biosynthesis of isoprenoid quinones and phenols in Gram-negative bacteria. Biochem. J. 111, 461-472.
32. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and, Provart, N. J., (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One, 2, e718.
33. Ye, C.Q., Folkers, K., Tamagawa, H., and, Pfeiffer, C., (1988) A modified determination of coenzyme Q10 in human blood and CoQ10 blood levels in diverse patients with allergies. Biofactors, 1, 303-306. (Pubitemid 19059460)
34. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and, van Wijk, K.J., (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One, 3, e1994.