Determination of 3-Hydroxy-3-methylglutaryl CoA Reductase Activity in Plants

  • Narciso Campos
  • Montserrat Arró
  • Albert Ferrer
  • Albert Boronat
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1153)

Abstract

The enzyme 3-hydroxy-3-methylglutaryl CoA (HMG-CoA) reductase catalyzes the NADPH-mediated reductive deacylation of HMG-CoA to mevalonic acid, which is the first committed step of the mevalonate pathway for isoprenoid biosynthesis. In agreement with its key regulatory role in the pathway, plant HMG-CoA reductase is modulated by many diverse external stimuli and endogenous factors and can be detected to variable levels in every plant tissue. A fine determination of HMG-CoA reductase activity levels is required to understand its contribution to plant development and adaptation to changing environmental conditions. Here, we report a procedure to reliably determine HMG-CoA reductase activity in plants. The method includes the sample collection and homogenization strategies as well as the specific activity determination based on a classical radiochemical assay.

Keywords

3-Hydroxy-3-methylglutaryl CoA reductase HMG-CoA reductase HMGR MVA Mevalonate pathway Isoprenoid Terpenoid 

Notes

Acknowledgment

This work was supported by grants of the Spanish Ministerio de Economía y Competitividad and the Spanish Ministerio de Ciencia e Innovación (BFU2011-24208 to N.C., BIO2009-06984 to A.F. and M.A., and BIO2009-09523 to A.B., including FEDER funds), the Spanish Consolider-Ingenio Program (CSD2007-00036 Centre for Research in Agrigenomics), and the Generalitat de Catalunya (2009SGR0026).

References

  1. 1.
    Rogers DH, Panini SR, Rudney H (1983) Properties of HMGCoA reductase and its mechanism of action. In: Sabine JR (ed) 3-hydroxy-3-methylglutaryl coenzyme A reductase. CRC, Boca Raton, FL, pp 57–75Google Scholar
  2. 2.
    Burg JS, Espenshade PJ (2011) Regulation of HMG-CoA reductase in mammals and yeast. Prog Lipid Res 50:403–410PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430PubMedCrossRefGoogle Scholar
  4. 4.
    Rodríguez-Concepción M, Campos N, Ferrer A et al (2013) Biosynthesis of isoprenoid precursors in Arabidopsis. In: Bach TJ, Rohmer M (eds) Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. Springer Science + Business Media, New York, pp 459–456Google Scholar
  5. 5.
    Bach TJ (1987) Synthesis and metabolism of mevalonic acid in plants. Plant Physiol Biochem 25:163–178Google Scholar
  6. 6.
    Stermer BA, Bianchini GM, Korth KL (1994) Regulation of HMG-CoA reductase activity in plants. J Lipid Res 35:1133–1140PubMedGoogle Scholar
  7. 7.
    Chappell J (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu Rev Plant Physiol Plant Mol Biol 46:521–547CrossRefGoogle Scholar
  8. 8.
    Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700. doi: 10.1146/annurev-arplant-050312-120116 PubMedCrossRefGoogle Scholar
  9. 9.
    Brooker JD, Russell DW (1979) Regulation of microsomal 3-hydroxy-3-methylglutaryl coenzyme A reductase from pea seedlings: Rapid posttranslational phytochrome-mediated decrease in activity and in vivo regulation by isoprenoid products. Arch Biochem Biophys 198:323–334PubMedCrossRefGoogle Scholar
  10. 10.
    Korth KL, Jaggard DAW, Dixon RA (2000) Developmental and light-regulated post-translational control of 3-hydroxy-3-methylglutaryl-CoA reductase levels in potato. Plant J 23:507–516PubMedCrossRefGoogle Scholar
  11. 11.
    Leivar P, Antolín-Llovera M, Ferrero S et al (2011) Multilevel control of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase by protein phosphatase 2A. Plant Cell 23:1494–1511PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Nieto B, Forés O, Arró M et al (2009) Arabidopsis 3-hydroxy-3-methylglutaryl-CoA reductase is regulated at the post-translational level in response to alterations of the sphingolipid and the sterol biosynthetic pathways. Phytochemistry 70:53–59PubMedCrossRefGoogle Scholar
  13. 13.
    Wentzinger LF, Bach TJ, Hartmann MA (2002) Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 130:334–346PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Russell DW, Knight JS, Wilson TM (1985) Pea seedling HMG-CoA reductases: regulation of activity in vitro by phosphorylation and Ca2+, and posttranslational control in vivo by phytochrome and isoprenoid hormones. In: Randall DD, Blevins DG, Larson RL, Kagawa T (eds) Current topics in plant biochemistry and physiology. University of Missouri-Columbia, Missouri, CO, pp 191–206Google Scholar
  15. 15.
    Wititsuwannakul R, Wititsuwannakul D, Dumkong S (1990) Hevea calmodulin: regulation of the activity of latex 3-hydroxy-3-methylglutaryl coenzyme A reductase. Phytochemistry 29:1755–1758CrossRefGoogle Scholar
  16. 16.
    Dale S, Arró M, Becerra B et al (1995) Bacterial expression of the catalytic domain of 3-hydroxy-3-methylglutaryl-CoA reductase (isoform HMGR1) from Arabidopsis thaliana, and its inactivation by phosphorylation at Ser577 by Brassica oleracea 3-hydroxy-3-methylglutaryl-CoA reductase kinase. Eur J Biochem 233:506–513PubMedCrossRefGoogle Scholar
  17. 17.
    Hemmerlin A (2013) Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Sci 203:41–54PubMedCrossRefGoogle Scholar
  18. 18.
    Sugden C, Donaghy PG, Halford NG et al (1999) Two SNF1-Related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol 120:257–274PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Antolín-Llovera M, Leivar P, Arró M et al (2011) Modulation of plant HMG-CoA reductase by protein phosphatase 2A: positive and negative control at a key node of metabolism. Plant Signal Behav 6:1127–1131PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Campos N, Boronat A (1995) Targeting and topology in the membrane of plant 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Cell 7:2163–2174PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Denbow CJ, Lang S, Cramer CL (1996) The N terminal domain of tomato 3-hydroxy-3-methylglutaryl-CoA reductases – sequence, microsomal targeting, and glycosylation. J Biol Chem 271:9710–9715PubMedCrossRefGoogle Scholar
  22. 22.
    Re EB, Brugger S, Learned M (1997) Genetic and biochemical analysis of the transmembrane domain of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase. J Cell Biochem 65:443–459PubMedCrossRefGoogle Scholar
  23. 23.
    Leivar P, González VM, Castel S et al (2005) Subcellular localization of Arabidopsis 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Plant Physiol 137:57–69PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Merret R, Cirioni JR, Bach TJ et al (2007) A serine involved in actin-dependent subcellular localization of a stress-induced tobacco BY-2 hydroxymethylglutaryl-CoA reductase isoform. FEBS Lett 581:5295–5299PubMedCrossRefGoogle Scholar
  25. 25.
    Kondo K, Oba K (1986) Purification and characterization of 3-hydroxy-3-methylglutaryl CoA reductase from potato tubers. J Biochem 100:967–974PubMedGoogle Scholar
  26. 26.
    Wititsuwannakul R, Wititsuwannakul D, Suwanmanee P (1990) 3-Hydroxy-3-methylglutaryl coenzyme A reductase from the latex of Hevea brasiliensis. Phytochemistry 29:1401–1403CrossRefGoogle Scholar
  27. 27.
    Bach TJ, Rogers DH, Rudney H (1986) Detergent-solubilization, purification, and characterization of membrane-bound 3-hydroxy-3-methylglutaryl-coenzyme-A reductase from radish seedlings. Eur J Biochem 154:103–111PubMedCrossRefGoogle Scholar
  28. 28.
    Choi D, Ward BL, Bostock RM (1992) Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell 4:1333–1344PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Chye ML, Kush A, Tan CT et al (1991) Characterization of cDNA and genomic clones encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase from Hevea brasiliensis. Plant Mol Biol 16:567–577PubMedCrossRefGoogle Scholar
  30. 30.
    Vollack KU, Dittrich B, Ferrer A et al (1994) Two radish genes for 3-hydroxy-3-methylglutaryl-CoA reductase isozymes complement mevalonate auxotrophy in a yeast mutant and yield membrane-bound active enzyme. J Plant Physiol 143:479–487CrossRefGoogle Scholar
  31. 31.
    Istvan ES, Palnitkar M, Buchanan SK et al (2000) Crystal structure of the catalytic portion of human HMG-CoA reductase: insights into regulation of activity and catalysis. EMBO J 19:819–830PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Lynen F (1967) Biosynthetic pathways from acetate to natural products. Pure Appl Chem 14:137–167PubMedCrossRefGoogle Scholar
  33. 33.
    Hepper CM, Audley BG (1969) Biosynthesis of rubber from β-hydroxy-β-methylglutaryl-coenzyme A in Hevea brasiliensis latex. Biochem J 114:379–386PubMedCentralPubMedGoogle Scholar
  34. 34.
    Brooker JD, Russell DW (1974) Some properties of 3-hydroxy-3-methylglutaryl coenzyme A reductase from Pisum sativum. Bull Roy Soc New Zeal 12:365–370Google Scholar
  35. 35.
    Suzuki H, Oba K, Uritani I (1974) Occurrence of 3-hydroxy-3-methyl-glutaryl coenzyme A reductase in sweet-potato. Agric Biol Chem 38:2053–2055CrossRefGoogle Scholar
  36. 36.
    Huber J, Rudiger W (1978) Subcellular localization and properties of 3-hydroxy-3-methylglutaryl coenzyme A reductase in plant cell suspension cultures of anise. Hoppe-Seylers Z Physiol Chem 359:277–277Google Scholar
  37. 37.
    Douglas TJ, Paleg LG (1978) AMO 1618 effects on incorporation of 14C-MVA and 14C-acetate into sterols in Nicotiana and Digitalis seedlings and cell-free preparations from Nicotiana. Phytochemistry 17:713–718CrossRefGoogle Scholar
  38. 38.
    Grumbach KH, Bach TJ (1979) Effect of PSII herbicides, amitrol and SAN 6706 on the activity of 3-hydroxy-3-methylglutaryl-coenzyme A reductase and the incorporation of [2-14C]acetate and [2-3H]mevalonate into chloroplast pigments of radish seedlings. Z Naturforsch (C) 34:941–943Google Scholar
  39. 39.
    Bach TJ, Wettstein A, Boronat A et al (1991) Properties and molecular cloning of plant HMG-CoA reductase. In: Patterson GW, Nes WD (eds) Physiology and biochemistry of plant sterols. American Oils Chemical Society, Champaign, IL, pp 29–49Google Scholar
  40. 40.
    Sipat A (1985) 3-Hydroxy-3-methylglutaryl-CoA reductase in the latex of Hevea brasiliensis. Methods Enzymol 110:40–51CrossRefGoogle Scholar
  41. 41.
    Sipat AB (1982) Hydroxymethylglutaryl CoA reductase (NADPH) in the latex of Hevea brasiliensis. Phytochemistry 21:2613–2618CrossRefGoogle Scholar
  42. 42.
    Suzuki H, Oba K, Uritani I (1975) The occurrence and some properties of 3-hydroxy-3-methylglutaryl coenzyme A reductase in sweet potato roots infected by Ceratocystis fimbriata. Physiol Plant Pathol 7:265–276CrossRefGoogle Scholar
  43. 43.
    Russell DW (1985) 3-Hydroxy-3-methylglutaryl-CoA reductases from pea seedlings. Methods Enzymol 110:26–40CrossRefGoogle Scholar
  44. 44.
    Reddy AR, Das VSR (1986) Partial purification and characterization of 3-hydroxy-3-methylglutaryl coenzyme A reductase from the leaves of guayule (Parthenium argentatum). Phytochemistry 25:2471–2474CrossRefGoogle Scholar
  45. 45.
    Shapiro DJ, Imblum RL, Rodwell VW (1969) Thin-layer chromatographic assay for HMG-CoA reductase and mevalonic acid. Anal Biochem 31:383PubMedCrossRefGoogle Scholar
  46. 46.
    Young NL, Berger B (1981) Assay of S-3-hydroxy-3-methylglutaryl-CoA reductase. Methods Enzymol 71(Pt C):498–509PubMedCrossRefGoogle Scholar
  47. 47.
    Chappell J, Wolf F, Proulx J et al (1995) Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plants ? Plant Physiol 109:1337–1343PubMedCentralPubMedGoogle Scholar
  48. 48.
    Dai Z, Cui G, Zhou S-F et al (2011) Cloning and characterization of a novel 3-hydroxy-3-methylglutaryl coenzyme A reductase gene from Salvia miltiorrhiza involved in diterpenoid tanshinone accumulation. J Plant Physiol 168:148–157PubMedCrossRefGoogle Scholar
  49. 49.
    Douglas P, Pigaglio E, Ferrer A et al (1997) Three spinach leaf nitrate reductase-3-hydroxy-3-methylglutaryl-CoA reductase kinases that are required by reversible phosphorylation and/or Ca2+ ions. Biochem J 325:101–109PubMedCentralPubMedGoogle Scholar
  50. 50.
    Mansouri H, Asrar Z, Mehrabani M (2009) Effects of gibberellic acid on primary terpenoids and D9-tetrahydrocannabinol in Cannabis sativa at flowering stage. J Integr Plant Biol 51:553–561PubMedCrossRefGoogle Scholar
  51. 51.
    Toroser D, Huber SC (1998) 3-Hydroxy-3-methylglutaryl-coenzyme A reductase kinase and sucrose-phosphate synthase kinase activities in cauliflower florets: Ca2+ dependence and substrate specificities. Arch Biochem Biophys 355:291–300PubMedCrossRefGoogle Scholar
  52. 52.
    Mozzicafreddo M, Cuccioloni M, Eleuteri AM et al (2010) Rapid reverse phase-HPLC assay of HMG-CoA reductase activity. J Lipid Res 51:2460–2463PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Soto G, Stritzler M, Lisi C et al (2011) Acetoacetyl-CoA thiolase regulates the mevalonate pathway during abiotic stress adaptation. J Exp Bot 62:5699–5711PubMedCrossRefGoogle Scholar
  54. 54.
    Waldron J, Webster C (2011) Liquid chromatography-tandem mass spectrometry method for the measurement of serum mevalonic acid: a novel marker of hydroxymethylglutaryl coenzyme A reductase inhibition by statins. Ann Clin Biochem 48:223–232PubMedCrossRefGoogle Scholar
  55. 55.
    Rodríguez-Concepción M, Forés O, Martínez-García JF et al (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16:144–156PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Closa M, Vranová E, Bortolotti C et al (2010) The Arabidopsis thaliana FPP synthase isozymes have overlapping and specific functions in isoprenoid biosynthesis, and complete loss of FPP synthase activity causes early developmental arrest. Plant J 63:512–525CrossRefGoogle Scholar
  57. 57.
    Manzano D, Fernàndez-Busquets X, Schaller H et al (2004) The metabolic imbalance underlying lesion formation in Arabidopsis thaliana overexpressing farnesyl diphosphate synthase (isoform 1S) leads to oxidative stress and is triggered by the developmental decline of endogenous HMGR activity. Planta 219:982–992PubMedCrossRefGoogle Scholar
  58. 58.
    Masferrer A, Arró M, Manzano D et al (2002) Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J 30:123–132PubMedCrossRefGoogle Scholar
  59. 59.
    Pastuszyn A, Havel CM, Scallen TJ et al (1983) (R)3-Hydroxy-3-methylglutaryl coenzyme A: the not-so-innocent bystander in the enzymatic reduction of (S)HMG-CoA to (R)mevalonate. J Lipid Res 24:1411–1411Google Scholar
  60. 60.
    Lalitha R, George R, Ramasarma T (1989) Mevalonate-metabolizing enzymes in Arachis hypogaea. Mol Cell Biochem 87:161–170PubMedCrossRefGoogle Scholar
  61. 61.
    Ram M, Khan MA, Jha P et al (2010) HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants. Acta Physiol Plant 32:859–866CrossRefGoogle Scholar
  62. 62.
    Narváez JA, Flores-Pérez P, Herrera-Valencia V et al (2001) Development of molecular techniques for studying the metabolism of carotenoids in Bixa orellana L. Hortscience 36:982–986Google Scholar
  63. 63.
    Harker M, Hellyer A, Clayton JC et al (2003) Co-ordinate regulation of sterol biosynthesis enzyme activity during accumulation of sterols in developing rape and tobacco seed. Planta 216:707–715PubMedGoogle Scholar
  64. 64.
    Kato-Emori S, Higashi K, Hosoya K et al (2001) Cloning and characterization of the gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase in melon (Cucumis melo L. reticulatus). Mol Genet Genomics 265:135–142PubMedCrossRefGoogle Scholar
  65. 65.
    Nishi A, Tsuritani I (1983) Effect of auxin on the metabolism of mevalonic acid in suspension-cultured carrot cells. Phytochemistry 22:399–401CrossRefGoogle Scholar
  66. 66.
    Golbeck JH, Maurey KM, Newberry GA (1985) Detection of 3 hydroxy-3-methylglutaryl coenzyme A reductase activity in Dunaliella salina. Plant Physiol 77:48Google Scholar
  67. 67.
    Skrukrud CL, Taylor SE, Hawkins DR et al (1987) Triterpenoid biosynthesis in Euphorbia lathyris. In: Stumpf PK, Mudd JB, Nes WD (eds) The metabolism, structure, and function of plant lipids. Plenum, New York, pp 115–118CrossRefGoogle Scholar
  68. 68.
    Skrukrud CL, Taylor SE, Hawkins DR et al (1988) Subcellular fractionation of triterpenoid biosynthesis in Euphorbia lathyris latex. Physiol Plant 74:306–316CrossRefGoogle Scholar
  69. 69.
    Leube J, Grisebach H (1983) Further studies on induction of enzymes of phytoalexin synthesis in soybean and cultured soybean cells. Z Naturforsch (C) 38:730–735Google Scholar
  70. 70.
    Joost O, Bianchini G, Bell AA et al (1995) Differential induction of 3-hydroxy-3-methylglutaryl CoA reductase in two cotton species following inoculation with Verticillium. Mol Plant Microbe Interact 8:880–885PubMedCrossRefGoogle Scholar
  71. 71.
    Ceccarelli N, Lorenzi R (1984) Growth inhibition by competitive inhibitors of 3-hydroxymethylglutarylcoenzyme A reductase in Helianthus tuberosus tissue explants. Plant Sci Lett 34:269–276CrossRefGoogle Scholar
  72. 72.
    Bach TJ (1981) Untersuchungen zur Charakterisierung und Regulation der 3-Hydroxy-3-methylglutaryl-Coenzym-A-Reduktase [Hydroxy-methylglutaryl-Coenzym-A Reduktase] (Mevalonat : NADP + Oxidoreduktase, CoA acylierend, E.C. 1.1.1.34) in Keimlingen von Raphanus sativus. Ph.D. Universität KarlsruheGoogle Scholar
  73. 73.
    Srinivasan V, Ryu DDY (1992) Enzyme activity and shikonin production in Lithospermum erythrorhizon cell cultures. Biotechnol Bioeng 40:69–74PubMedCrossRefGoogle Scholar
  74. 74.
    Köhle A, Sommer S, Yazaki K et al (2002) High level expression of chorismate pyruvate-lyase (UbiC) and HMG-CoA reductase in hairy root cultures of Lithospermum erythrorhizon. Plant Cell Physiol 43:894–902PubMedCrossRefGoogle Scholar
  75. 75.
    Rupasinghe HPV, Almquist KC, Paliyath G et al (2001) Cloning of hmg1 and hmg2 cDNAs encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase and their expression and activity in relation to alpha-farnesene synthesis in apple. Plant Physiol Biochem 39:933–947CrossRefGoogle Scholar
  76. 76.
    Arebalo RE, Mitchell ED (1984) Cellular distribution of 3-hydroxy-3-methylglutaryl coenzyme A reductase and mevalonate kinase in leaves of Nepeta cataria. Phytochemistry 23:13–18CrossRefGoogle Scholar
  77. 77.
    van Deenen N, Bachmann AL, Schmidt T et al (2012) Molecular cloning of mevalonate pathway genes from Taraxacum brevicorniculatum and functional characterisation of the key enzyme 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Mol Biol Rep 39:4337–4349PubMedCrossRefGoogle Scholar
  78. 78.
    Chappell J, Nable R (1987) Induction of sesquiterpenoid biosynthesis in tobacco cell suspension cultures by fungal elicitor. Plant Physiol 85:469–473PubMedCentralPubMedCrossRefGoogle Scholar
  79. 79.
    Gondet L, Weber T, Maillotvernier P et al (1992) Regulatory role of microsomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase in a tobacco mutant that overproduces sterols. Biochem Biophys Res Commun 186:888–893PubMedCrossRefGoogle Scholar
  80. 80.
    Maurey K, Wolf F, Golbeck J (1986) 3-Hydroxy-3-Methylglutaryl Coenzyme A reductase activity in Ochromonas malhamensis: a system to study the relationship between enzyme activity and rate of steroid biosynthesis. Plant Physiol 82:523–527PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Ji W, Benedict CR, Foster MA (1993) Seasonal variations in rubber biosynthesis, 3-hydroxy-3-methylglutaryl-coenzyme A reductase, and rubber transferase activities in Parthenium argentatum in the chihuahuan desert. Plant Physiol 103:535–542PubMedCentralPubMedGoogle Scholar
  82. 82.
    Cowan AK, MooreGordon CS, Bertling I et al (1997) Metabolic control of avocado fruit growth – Isoprenoid growth regulators and the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 114:511–518PubMedCentralPubMedGoogle Scholar
  83. 83.
    Cowan AK (2004) Metabolic control of avocado fruit growth: 3-hydroxy-3-methylglutaryl coenzyme a reductase, active oxygen species and the role of C7 sugars. S Afr J Bot 70:75–82Google Scholar
  84. 84.
    Reddy AR, Das VSR (1987) Chloroplast autonomy for the biosynthesis of isopentenyl diphosphate in guayule (Parthenium argentatum gray). New Phytol 106:457–464CrossRefGoogle Scholar
  85. 85.
    Boll M, Kardinal A (1990) 3-Hydroxy-3-methylglutaryl coenzyme A reductase from spruce (Picea abies). Properties and regulation. Z Naturforsch (C) 45:973–979Google Scholar
  86. 86.
    Lütke-Brinkhaus F, Kleinig H (1987) Formation of isopentenyl diphosphate via mevalonate does not occur within etioplasts and etiochloroplasts of mustard Sinapis alba L. seedlings. Planta 171:406–411PubMedCrossRefGoogle Scholar
  87. 87.
    Narita JO, Gruissem W (1989) Tomato hydroxymethylglutaryl-CoA reductase is required early in fruit development but not during ripening. Plant Cell 1:181–190PubMedCentralPubMedCrossRefGoogle Scholar
  88. 88.
    Oba K, Kondo K, Doke N et al (1985) Induction of 3-hydroxy-3-methylglutaryl CoA reductase in potato tubers after slicing, fungal infection or chemical treatment, and some properties of the enzyme. Plant Cell Physiol 26:873–880Google Scholar
  89. 89.
    Josekutty PC (1998) Selection and characterization of Solanum xanthocarpum cell line with augmented steroid metabolism. S Afr J Bot 64:238–243Google Scholar
  90. 90.
    Kreuz K, Kleinig H (1984) Synthesis of prenyl lipids in cells of spinach leaf. Compartmentation of enzymes for formation of isopentenyl diphosphate. Eur J Biochem 141:531–535PubMedCrossRefGoogle Scholar
  91. 91.
    Kim KK, Yamashita H, Sawa Y et al (1996) A high activity of 3-hydroxy-3-methylglutaryl coenzyme a reductase in chloroplasts of Stevia rebaudiana Bertoni. Biosci Biotechnol Biochem 60:685–686CrossRefGoogle Scholar
  92. 92.
    Post J, van Deenen N, Fricke J et al (2012) Laticifer-specific cis-prenyltransferase silencing affects the rubber, triterpene, and inulin content of Taraxacum brevicorniculatum. Plant Physiol 158:1406–1417PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Bach TJ, Weber T, Motel A (1990) Some properties of enzymes involved in the biosynthesis and metabolism of 3-hydroxy-3-methylglutaryl-CoA in plants. In: Towers GHN, Stafford HA (eds) Biochemistry of the mevalonic acid pathway to terpenoids. Plenum Press Div Plenum Publishing Corp, New York, pp 1–82CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Narciso Campos
    • 1
    • 2
  • Montserrat Arró
    • 1
    • 3
  • Albert Ferrer
    • 1
    • 3
  • Albert Boronat
    • 1
    • 2
  1. 1.Center for Research in Agricultural Genomics (CRAG)CSIC-IRTA-UAB-UBBarcelonaSpain
  2. 2.Department of Biochemistry and Molecular Biology, Faculty of PharmacyUniversity of BarcelonaBarcelonaSpain
  3. 3.Faculty of Pharmacy, Department of Biochemistry and Molecular BiologyUniversity of BarcelonaBarcelonaSpain

Personalised recommendations