The origin and biosynthesis of the benzenoid moiety of ubiquinone (Coenzyme Q) in Arabidopsis

Plant Cell

Volumn 26, Issue 5, 2014, Pages 1938-1948

  Block, Anna ^a   Widhalm, Joshua R ^b   Fatihi, Abdelhak ^a   Cahoon, Rebecca E ^a   Wamboldt, Yashitola ^a   Elowsky, Christian ^a   Mackenzie, Sally A ^a   Cahoon, Edgar B ^a   Chapple, Clint ^b   Dudareva, Natalia ^b   Basset, Gilles J ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903581554     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.125807     Document Type: Article

References (52)

1. Achnine, L., Blancaflor, E.B., Rasmussen, S., and Dixon, R.A. (2004). Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16: 3098-3109.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. 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.
4. Block, A., Fristedt, R., Rogers, S., Kumar, J., Barnes, B., Barnes, J., Elowsky, C.G., Wamboldt, Y., Mackenzie, S.A., Redding, K., Merchant, S.S., and Basset, G.J. (2013). Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids. J. Biol. Chem. 288: 27594-27606.
5. 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.
6. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
7. Bussell, J.D., Reichelt, M., Wiszniewski, A.A., Gershenzon, J., and Smith, S.M. (2014). Peroxisomal ATP-binding cassette transporter COMATOSE and the multifunctional protein abnormal INFLORESCENCE MERISTEM are required for the production of benzoylated metabolites in Arabidopsis seeds. Plant Physiol. 164: 48-54.
8. Cardazzo, B., Hamel, P., Sakamoto, W., Wintz, H., and Dujardin, G. (1998). Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity. Gene 221: 117-125.
9. Clarke, C.F. (2000). New advances in coenzyme Q biosynthesis. Protoplasma 213: 134-147.
10. 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.
11. Colquhoun, T.A., Marciniak, D.M., Wedde, A.E., Kim, J.Y., Schwieterman, M.L., Levin, L.A., Van Moerkercke, A., Schuurink, R.C., and Clark, D.G. (2012). A peroxisomally localized acyl-activating enzyme is required for volatile benzenoid formation in a Petunia3hybrida cv. 'Mitchell Diploid' flower. J. Exp. Bot. 63: 4821-4833.
12. Costa, M.A., et al. (2005). Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation. Phytochemistry 66: 2072-2091.
13. Dawson, R.M.C., Elliot, D.C., Elliot, W.H., and Jones, K.M. (1986). Data for Biochemical Research. (New York: Oxford University Press).
14. DellaPenna, D., and Pogson, B.J. (2006). Vitamin synthesis in plants: tocopherols and carotenoids. Annu. Rev. Plant Biol. 57: 711-738.
15. De Marcos Lousa, C., van Roermund, C.W., Postis, V.L., Dietrich, D., Kerr, I.D., Wanders, R.J., Baldwin, S.A., Baker, A., and Theodoulou, F.L. (2013). Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids. Proc. Natl. Acad. Sci. USA 110: 1279-1284.
16. Ducluzeau, A.-L., Wamboldt, Y., Elowsky, C.G., Mackenzie, S.A., Schuurink, R.C., and Basset, G.J.C. (2012). 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.
17. Egland, P.G., and Harwood, C.S. (2000). HbaR, a 4-hydroxybenzoate sensor and FNR-CRP superfamily member, regulates anaerobic 4-hydroxybenzoate degradation by Rhodopseudomonas palustris. J. Bacteriol. 182: 100-106.
18. Ehlting, J., Büttner, D., Wang, Q., Douglas, C.J., Somssich, I.E., and Kombrink, E. (1999). Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 19: 9-20.
19. Footitt, S., Slocombe, S.P., Larner, V., Kurup, S., Wu, Y., Larson, T., Graham, I., Baker, A., and Holdsworth, M. (2002). Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21: 2912-2922.
20. Forner, J., and Binder, S. (2007). The red fluorescent protein eqFP611: application in subcellular localization studies in higher plants. BMC Plant Biol. 7: 28.
21. Gaid, M.M., Sircar, D., Müller, A., Beuerle, T., Liu, B., Ernst, L., Hänsch, R., and Beerhues, L. (2012). Cinnamate:CoA ligase initiates the biosynthesis of a benzoate-derived xanthone phytoalexin in Hypericum calycinum cell cultures. Plant Physiol. 160: 1267-1280.
22. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994.
23. Hamberger, B., and Hahlbrock, K. (2004). The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc. Natl. Acad. Sci. USA 101: 2209-2214.
24. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
25. Kawamukai, M. (2009). Biosynthesis and bioproduction of coenzyme Q10 by yeasts and other organisms. Biotechnol. Appl. Biochem. 53: 217-226.
26. Kienow, L., Schneider, K., Bartsch, M., Stuible, H.P., Weng, H., Miersch, O., Wasternack, C., and Kombrink, E. (2008). Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana. J. Exp. Bot. 59: 403-419.
27. Klempien, A., et al. (2012). Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers. Plant Cell 24: 2015-2030.
28. Kliebenstein, D.J., D'Auria, J.C., Behere, A.S., Kim, J.H., Gunderson, K.L., Breen, J.N., Lee, G., Gershenzon, J., Last, R.L., and Jander, G. (2007). Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J. 51: 1062-1076.
29. Koo, A.J.K., Chung, H.S., Kobayashi, Y., and Howe, G.A. (2006). Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. J. Biol. Chem. 281: 33511-33520.
30. Law, A.H., Threlfall, D.R., and Whistance, G.R. (1971). Isoprenoid phenol and quinone precursors of ubiquinones and dihydroubiquinones [Ubiquinones (H2)] in fungi. Biochem. J. 123: 331-339.
31. Lee, D., Meyer, K., Chapple, C., and Douglas, C.J. (1997). Antisense suppression of 4-coumarate:coenzyme A ligase activity in Arabidopsis leads to altered lignin subunit composition. Plant Cell 9: 1985-1998.
32. Lee, S., Kaminaga, Y., Cooper, B., Pichersky, E., Dudareva, N., and Chapple, C. (2012). Benzoylation and sinapoylation of glucosinolate R-groups in Arabidopsis. Plant J. 72: 411-422.
33. Löscher, R., and Heide, L. (1994). Biosynthesis of p-hydroxybenzoate from p-coumarate and p-coumaroyl-CoA in cell-free extracts of Lithospermum erythrorhizon cell cultures. Plant Physiol. 106: 271-279.
34. Marbois, B., Xie, L.X., Choi, S., Hirano, K., Hyman, K., and Clarke, C.F. (2010). para-Aminobenzoic acid is a precursor in coenzyme Q6 biosynthesis in Saccharomyces cerevisiae. J. Biol. Chem. 285: 27827-27838.
35. Nichols, B.P., and Green, J.M. (1992). Cloning and sequencing of Escherichia coli ubiC and purification of chorismate lyase. J. Bacteriol. 174: 5309-5316.
36. Nowicka, B., and Kruk, J. (2010). Occurrence, biosynthesis and function of isoprenoid quinones. Biochim. Biophys. Acta 1797: 1587-1605.
37. 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.
38. 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.
39. Olson, R.E., Bentley, R., Aiyar, A.S., Dialameh, G.H., Gold, P.H., Ramsey, V.G., and Springer, C.M. (1963). Benzoate derivatives as intermediates in the biosynthesis of coenzyme Q in the rat. J. Biol. Chem. 238: 3146-3148.
40. Pierrel, F., Hamelin, O., Douki, T., Kieffer-Jaquinod, S., Mühlenhoff, U., Ozeir, M., Lill, R., and Fontecave, M. (2010). Involvement of mitochondrial ferredoxin and para-aminobenzoic acid in yeast coenzyme Q biosynthesis. Chem. Biol. 17: 449-459.
41. Pribat, A., et al. (2010). Nonflowering plants possess a unique folatedependent phenylalanine hydroxylase that is localized in chloroplasts. Plant Cell 22: 3410-3422.
42. Qualley, A.V., Widhalm, J.R., Adebesin, F., Kish, C.M., and Dudareva, N. (2012). Completion of the core b-oxidative pathway of benzoic acid biosynthesis in plants. Proc. Natl. Acad. Sci. USA 109: 16383-16388.
43. Quinlivan, E.P., Roje, S., Basset, G., Shachar-Hill, Y., Gregory, J.F., III., and Hanson, A.D. (2003). The folate precursor p-aminobenzoate is reversibly converted to its glucose ester in the plant cytosol. J. Biol. Chem. 278: 20731-20737.
44. Pfaff, C., Glindemann, N., Gruber, J., Frentzen, M., and Sadre, R. (2014). Chorismate pyruvate-lyase and 4-hydroxy-3-solanesylbenzoate decarboxylase are required for plastoquinone biosynthesis in the cyanobacterium Synechocystis sp. PCC6803. J. Biol. Chem. 289: 2675-2686.
45. Reumann, S. (2013). Biosynthesis of vitamin k1 (phylloquinone) by plant peroxisomes and its integration into signaling molecule synthesis pathways. Subcell. Biochem. 69: 213-229.
46. Richmond, T.A., and Bleecker, A.B. (1999). A defect in beta-oxidation causes abnormal inflorescence development in Arabidopsis. Plant Cell 11: 1911-1924.
47. Robinson, S.J., et al. (2009). An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches. BMC Plant Biol. 9: 101.
48. Schilmiller, A.L., Stout, J., Weng, J.K., Humphreys, J., Ruegger, M.O., and Chapple, C. (2009). Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J. 60: 771-782.
49. Shockey, J., and Browse, J. (2011). Genome-level and biochemical diversity of the acyl-activating enzyme superfamily in plants. Plant J. 66: 143-160.
50. Van Moerkercke, A., Schauvinhold, I., Pichersky, E., Haring, M.A., and Schuurink, R.C. (2009). A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. Plant J. 60: 292-302.
51. Widhalm, J.R., Ducluzeau, A.-L., Buller, N.E., Elowsky, C.G., Olsen, L.J., and Basset, G.J.C. (2012). Phylloquinone (vitamin K(1) biosynthesis in plants: two peroxisomal thioesterases of lactobacillales origin hydrolyze 1,4-dihydroxy-2-naphthoyl-coa. Plant J. 71: 205-215.
52. Zolman, B.K., Silva, I.D., and Bartel, B. (2001). The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid b-oxidation. Plant Physiol. 127: 1266-1278.