HOME JOURNALS CONTACT

Journal of Biological Sciences

Year: 2006 | Volume: 6 | Issue: 1 | Page No.: 209-219
DOI: 10.3923/jbs.2006.209.219
Isoprenoid Biosynthesis in Plants: Pathways, Genes, Regulation and Metabolic Engineering
Zhi-Hua Liao, Min Chen, Yi-Fu Gong, Zhi-Qi Miao, Xiao-Fen Sun and Ke-Xuan Tang

Abstract: Isoprenoids, namely terpenoids, are the largest and the most structurally varied groups of natural products, which contain more than 30,000 known compounds. All the isoprenoids are biosynthesized from only two C5 precursors in plants, isopentenyl diphosphate and its isomer, dimethylallyl diphosphate. Two distinct pathways of isopentenyl diphosphate biosynthesis exist in plants: the classical mevalonate pathway and the recently unveiled deoxyxylulose 5-phosphate pathway. In this study, we summarize the recent progress on the molecular genetics of the two pathways, specializing in pathways, genes, enzymes, intermediates, subcellular compartments of isoprenoid biosynthesis, crosstalk of the two pathways and metabolic regulation and engineering.

Fulltext PDF

How to cite this article
Zhi-Hua Liao, Min Chen, Yi-Fu Gong, Zhi-Qi Miao, Xiao-Fen Sun and Ke-Xuan Tang, 2006. Isoprenoid Biosynthesis in Plants: Pathways, Genes, Regulation and Metabolic Engineering. Journal of Biological Sciences, 6: 209-219.

Keywords: Biosynthesis, gene, isoprenoid, metabolic engineering, pathway and regulation

REFERENCES

  • Hartmann, T., 1996. Diversity and variability of plant secondary metabolism: A mechanistic view. Entomol. Gen. Appl., 80: 177-188.
    CrossRef    


  • Croteau, R., T.M. Kutchan and N.G. Lewis, 2000. Natural Products (Secondary Metabolites). In: Biochemistry and Molecular Biology of Plants, Buchanan, B.B., W. Gruissem and R.L. Jones (Eds.). American Society of Plant Physiologists, Rockville, Maryland, USA., pp: 1250-1318


  • Wani, M.C., H.L. Taylor, M.E. Wall, P. Coggon and A.T. McPhail, 1971. Plant antitumor agents VI the isolation and structure of taxol a novel antileukemic and antitumor agent from us brevifolia. J. Am. Chem. Soc., 93: 2325-2327.
    PubMed    


  • Chen, X.Y. and Z.H. Xu, 1996. Recent progress in biotechnology and genetic engineering of medicinal plants in China. Med. Chem. Res., 6: 215-224.


  • Cieza, A., P. Maier and E. Poppel, 2003. The effect of Ginkgo Biloba on healthy elderly subjects. Fortschritte Der Medzin, 1: 10-15.
    PubMed    


  • Dewick, P.M., 2002. The biosynthesis of C 5 BC 25 terpenoid compounds. Nat. Prod. Rep., 19: 181-222.


  • Bick, J.A. and B.M. Lange, 2003. Metabolic crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis Unidirectional transport of intermediates across the chloroplast envelope membrane. Arch. Biochem. Biophys., 415: 146-154.
    PubMed    


  • Igual, J.C., C.G. Bosch, J. Dopazo and J.E.P. Ortin, 1992. Phylogenetic analysis of the thiolase family implications for the evolutionary origin of peroxisomes. J. Mol. Evol., 35: 147-155.
    PubMed    


  • Luskey, K.L. and B. Stevens, 1985. Human 3 hydroxy 3 methylglutaryl coenzyme a reductase conserved domains responsible for catalytic activity and sterol regulated degradation. J. Biol. Chem., 260: 10271-10277.
    Direct Link    


  • Basson, M.E., M. Thorsness, J.F. Moore, R.M. Stroud and J. Rine, 1988. Structural and functional conservation between yeast and human 3 hydroxy 3 methylglutaryl coenzyme a reductases the rate limiting enzyme of sterol biosynthesis. Mol. Cell. Biol., 8: 3797-3808.
    Direct Link    


  • Lluch, M.A., A. Masferrer, M. Arro, A. Boronat and A. Ferrer, 2000. Molecular cloning and expression analysis of the mevalonate kinase gene from Arabidopsis thaliana. Plant Mol. Biol., 42: 365-376.
    PubMed    


  • Tsay, Y.H. and G.W. Robinson, 1991. Cloning and characterization of ERG8 an essential gene of Saccharomyces cerevisiae that encodes phosphomevalonate kinase. Mol. Cell Biol., 11: 620-631.
    Direct Link    


  • Paganon, S.D., J. Magrath and R.H. Abeles, 1994. Mechanism of mevalonate pyrophosphate decarboxylase evidence for a carbocationic transition state. Biochemistry, 33: 133551-133562.
    PubMed    


  • Wouters, J., Y. Oudjama, S. Ghosh, V. Stalon, L. Droogmans and E. Oldfield, 2003. Structure and mechanism of action of isopentenylpyrophosphate dimethylallylpyrophosphate isomerase. J. Am. Chem. Soc., 125: 3198-3199.
    CrossRef    


  • Disch, A., A. Hemmerlin, T.J. Bach and M. Rohmer, 1998. Mevalonate derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY 2 cells. Biochem. J., 331: 615-621.


  • Rohmer, M., M. Knani, P. Simonin, B. Sutter and H. Sahm, 1993. Isoprenoid biosynthesis in bacteria a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J., 295: 517-524.


  • Schwarz, M.K., 1994. Terpen biosynthese in Ginkgo biloba eine uberraschende Geschichte. Ph.D. Thesis, ETH, Zurich, Switzerland.


  • Sprenger, G.A., U. Schorken, T. Wiegert, S. Grolle and H. Sahm et al., 1997. Identification of a thiamin dependent synthase in Escherichia coli required for the formation of the 1 deoxy D xylulose 5 phosphate precursor to isoprenoids thiamin and pyridoxol. Proc. Natl. Acad. Sci. USA., 94: 12857-12862.
    Direct Link    


  • Juan, M., E.A. Cantero, A. Reindl, S. Reichler and P. Leon, 2001. 1 deoxy D xylulose 5 phosphate synthase a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem., 276: 22901-22909.
    Direct Link    


  • Takahashi, S., T. Kuzuyama, H. Watanabe and H. Seto, 1998. A 1 deoxy D xylulose 5 phosphate reductoisomerase catalyzing the formation of 2 C methyl D erythritol 4 phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Nat. Acad. Sci. USA., 95: 9879-9884.


  • Rohdich, F., J. Wungsintaweekul, W. Eisenreich, G. Richter and A. Bacher et al., 2000. Biosynthesis of terpenoids 4 diphosphocytidyl 2C methyl D erythritol synthase of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA., 97: 6451-6456.
    Direct Link    


  • Steinbacher, S., J. Kaiser, W. Eisenreich, R. Huber, A. Bacher and F. Rohdich, 2003. Structural basis of fosmidomycin action revealed by the complex with 2 C methyl D erythritol 4 phosphate synthase (IspC) implications for the catalytic mechanism and anti malaria drug development. J. Biol. Chem., 278: 18401-18407.
    CrossRef    


  • Herz, S., J. Wungsintaweekul, C.A. Schuhr, S. Hecht and F. Rohdich et al., 2000. Biosynthesis of terpenoids YgbB protein converts 4 diphosphocytidyl 2C methyl D erythritol 2 phosphate to 2C methyl D erythritol 2 4 cyclodiphosphate. Proc. Natl. Acad. Sci. USA., 97: 2486-2490.
    PubMed    


  • Baker, J., D.B. Franklin and J. Parker, 1992. Sequence and characterization of the gcpE gene of Escherichia coli. FEMS Microbiol. Lett., 73: 175-180.
    PubMed    


  • Cunningham, F.X., T.P. Lafond and E. Gantt, 2000. Evidence of a role for LytB in the nonmevalonate pathway of isoprenoid biosynthesis. J. Bacteriol., 182: 5841-5848.


  • Montamat, F., M. Guilloton, F. Karst and S. Delrot, 1995. Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3 hydroxy 3 methylglutaryl coenzyme a synthase. Gene, 167: 197-201.


  • Vollack, K.U. and T.J. Bach, 1996. Cloning of a cDNA encoding cytosolic acetoacetyl coenzyme a thiolase from radish by functional expression in Saccharomyces cerevisiae. Plant Physiol., 111: 1097-1107.
    Direct Link    


  • Rokosz, L.L., D.A. Boulton, E.A. Butkiewicz, G. Sanyal, M.A. Cueto, P.A. Lachance and J.D. Hermes, 1994. Human cytoplasmic 3 hydroxy 3 methylglutaryl coenzyme a synthase expression purification and characterization of recombinant wild type and Cys(129) mutant enzymes. Arch. Biochem. Biophys., 312: 1-13.
    Direct Link    


  • Alex, D., T.J. Bach and M.L. Chye, 2000. Expression of Brassica junceaa 3 hydroxy 3 methylglutaryl Co synthase is developmentally regulated and stress responsive. Plant J., 22: 415-426.
    Direct Link    


  • Wegener, A., W. Gimbel, T. Werner, J. Hani, D. Ernst and H.J. Sandermann, 1997. Molecular cloning of ozone inducible protein from Pinus sylvestris L. with high sequence similarity to vertebrate 3 hydroxy 3 methylglutaryl Coa synthase. Biochem. Biophys. Acta, 1350: 247-252.
    PubMed    


  • Suwanmanee, P., N. Sirinupong and W. Suvachittanont, 2004. Regulation of the expression of 3 hydroxy 3 methylglutaryl CoA synthase gene in Hevea brasiliensis (BHK) Mull. Arg. Plant Sci., 166: 531-537.
    Direct Link    


  • Caelles, C., A. Ferrer, L. Balcells, F.G. Hegardt and A. Boronat, 1989. Isolation and structural characterization of a cDNA encoding Arabidopsis thaliana 3 hydroxy 3 methylglutaryl coenzyme a reductase. Plant Mol. Biol., 13: 627-638.


  • Istvan, E.S. and J. Deisenhofer, 2000. The structure of the catalytic portion of human HMG Coa reductase. Biochem. Biophys. Acta, 1529: 9-18.
    PubMed    


  • Albert, J.R., E.C. Olmedo and L.M. Corrochano, 2001. Genes for mevalonate biosynthesis in Phycomyces. Mol. Genet. Gen., 266: 768-777.


  • Suzuki, M., Y. Kamide, N. Nagata, H. Seki and T. Muranaka et al., 2004. Loss of function of 3 hydroxy 3 methylglutaryl coenzyme a reductase 1 (HMG1) in Arabidopsis leads to dwarfing early senescence and male sterility and reduced sterol levels. Plant J., 37: 750-761.
    PubMed    


  • Mendoza, I.E.M., R.M. Vincent and C.L. Nessler, 1997. Molecular characterization of three differentially expressed members of the Camptotheca acuminata 3 hydroxy 3 methylglutaryl CoA reductase (HMGR) gene family. Plant Mol. Biol., 34: 781-790.


  • Mendoza, I.E.M., R.J. Burnett and C.L. Nessler, 1992. Nucleotide sequence of a cDNA encoding 3 hydroxy 3 methylglutaryl coenzyme a reductase from Catharanthus roseus. Plant Physiol., 100: 1613-1614.
    Direct Link    


  • Emori, S.K., K. Higashi, K. Hosoya, T. Kobayashi and H. Ezura, 2001. Cloning and characterization of the gene encoding 3 hydroxy 3 methylglutaryl coenzyme a reductase in melon (Cucumis melo L. Reticulatus). Mol. Genet. Gen., 265: 135-142.
    Direct Link    


  • Park, H., C.J. Denbow and C.L. Cramer, 1992. Structure and nucleotide sequence of tomato HMG2 encoding 3 hydroxy 3 methyl glutaryl coenzyme a reductase. Plant Mol. Biol., 20: 327-331.
    CrossRef    


  • Learned, R.M. and G.R. Fink, 1989. 3 Hydroxy 3 methylglutaryl coenzyme a reductase from Arabidopsis thaliana is structurally distinct from the yeast and animal enzymes. Proc. Nat. Acad. Sci. USA., 86: 2779-2783.
    Direct Link    


  • Liao, Z.H., Q.M. Tan, Y.R. Chai, K.J. Zuo and K.X. Tang et al., 2003. Cloning and characterization of the gene encoding HMG Coa reductase from Taxus media and its functional identification in yeast. Funct. Plant Biol., 31: 73-81.
    Direct Link    


  • Chye, M.L., C.T. Tan and H.H. Chua, 1992. Three genes encode 3 hydroxy 3 methylglutaryl coenzyme a reductase in Hevea brasiliensis, hmg1 and hmg3 are differentially expressed. Plant Mol. Biol., 19: 473-484.
    Direct Link    


  • Bach, T.J., 1995. Some new aspects of isoprenoid biosynthesis in plants a review. Lipids, 30: 191-202.
    CrossRef    


  • Lee, M. and T. Leustek, 1999. Identification of the gene encoding homoserine kinase from Arabidopsis thaliana and characterization of the recombinant enzyme derived from the gene. Arch. Biochem. Biophys., 372: 135-142.


  • Cordier, H., F. Karst and T. Berges, 1999. Heterologous expression in saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol. Biol., 39: 953-967.
    PubMed    


  • Cunningham, F.X.J. and E. Gantt, 2000. Identification of multi gene families encoding isopentenyl diphosphate isomerase in plants by heterologous complementation in Escherichia coli. Plant Cell. Physiol., 41: 119-123.
    Direct Link    


  • Aboushadi, N., W.H. Engfelt, V.G. Paton and S.K. Krisans, 1999. Role of peroxisomes in isoprenoid biosynthesis. J. Histochem. Cytochem., 47: 1127-1132.
    Direct Link    


  • Valdivia, A.C.R., R.V. Heijden and R. Verpoorte, 1997. Isopentenyl diphosphate isomerase a core enzyme in isoprenoid biosynthesis a review of its biochemistry and function. Natl. Prod. Rep., 14: 591-603.
    PubMed    


  • Lois, L.M., M.R. Concepcion, F. Gallego, N. Campos and A. Boronat, 2000. Carotenoid biosynthesis during tomato fruit development regulatory role of 1deoxy D xylulose 5 phosphate synthase. Plant J., 22: 503-513.


  • Bouvier, F., A.D. Harlingue, C. Suire, R.A. Backhaus and B. Camara, 1998. Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant Physiol., 117: 1423-1431.


  • Souret, F.D.F., P.J. Weathers and K.K. Wobbe, 2002. The mevalonate independent pathway is expressed in transformed roots of artemisia annua and regulated by light and culture age. In vitro Cell. Dev. Biol. Plant, 38: 581-588.


  • Okuhara, M., Y. Kuroda, T. Goto, M. Okamoto and H. Imanaka et al., 1980. Studies on new phosphonic acid antibiotics III Isolation and characterization of FR 31564 FR 32863 and FR 33289 So DXR is the new target protein for developing new herbicides. J. Antibiot., 33: 24-28.


  • Lange, B.M., R.E.B. Ketchum and R.B. Croteau, 2001. Isoprenoid biosynthesis metabolite profiling of peppermint oil gland secretory cells and application to herbicide target analysis. Plant Physiol., 127: 305-314.
    CrossRef    PubMed    


  • Markus L., B., T. Rujan, W. Martin and R. Croteau, 2000. Isoprenoid biosynthesis the evolution of two ancient and distinct pathways across genomes. Proc. Nat. Acad. Sci. USA., 97: 13172-13177.


  • Paulet, L.C., I. Ahumada, N. Cunillera, M.R. Concepcion, A. Ferrer, A. Boronat and N. Campos, 2002. Expression and molecular analysis of the Arabidopsis DXR gene encoding 1 deoxy D xylulose 5 phosphate reductoisomerase the first committed enzyme of the 2 C methyl D erythritol 4 phosphate pathway. Plant Physiol., 129: 1581-1591.
    Direct Link    


  • Veau, B., M. Courtois, A. Oudin, J.C. Chenieux, M. Rideau and M. Clastre, 2000. Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochem. Biophys. Acta Gen. St. Exp., 1517: 159-163.


  • Rohdich, F., J. Wungsintaweekul, H. Luttgen, M. Fischer and A. Bacher et al., 2000. Biosynthesis of isoprenoids 4 diphosphocytidyl 2 cmethyl D erythritol kinase from tomato. Proc. Natl. Acad. Sci. USA., 97: 8251-8256.


  • Kishida, H., T. Wada, S. Unzai, T. Kuzuyama and S.Y. Park et al., 2003. Structure and catalytic mechanism of 2 C methyl D erythritol 2 4 cyclodiphosphate (MECDP) synthase an enzyme in the non mevalonate pathway of isoprenoid synthesis. Acta Crystallogr. D. Biol. Crystallogr., 59: 23-31.


  • Altincicek, B., A.K. Kollas, S. Sanderbrand, J. Wiesner, M. Hintz, E. Beck and H. Jomaa, 2001. GcpE is involved in the 2 C methyl D erythritol 4 phosphate pathway of isoprenoid biosynthesis in Escherichia coli. J. Bacteriol., 183: 2411-2416.


  • Querol, J., N. Campos, S. Imperial, A. Boronat and M.R. Concepcion, 2002. Functional analysis of the Arabidopsis thaliana GCPE protein involved in plastid isoprenoid biosynthesis. FEBS Lett., 514: 343-346.


  • Concepeion, M.R., J. Querol, L.M. Lois, S. Imperial and A. Boronat, 2003. Bioinformatic and molecular analysis of hydroxymethylbutenyl diphosphate synthase (GCPE) gene expression during carotenoid accumulation in ripening tomato fruit. Planta, 217: 476-482.


  • Rohdich, F., S. Hecht, K. Gartner, P. Adam and W. Eisenreich et al., 2002. Studies on the nonmevalonate terpene biosynthetic pathway metabolic role of IspH (LytB) protein. Proc. Natl. Acad. Sci. USA., 99: 1158-1163.


  • Page, J.E., G. Hause, M. Raschke, W.Y. Gao, J. Schmidt, M.H. Zenk and T.M. Kutchan, 2004. Functional analysis of the final steps of the 1 Deoxy D xylulose 5 phosphate (DXP) pathway to isoprenoids in plants using virusinduced gene silencing. Plant Physiol., 134: 1401-1413.


  • Adam, K.P. and J. Zapp, 1998. Biosynthesis of the isoprene units of chamomile sesquiterpenes. Phytochemistry, 48: 953-959.


  • Wang, Y.D., Y.J. Yuan, M. Lu, J.C. Wu and J.L. Jiang, 2003. Inhibitor studies of isopentenyl pyrophosphate biosynthesis in suspension cultures of the new Taxus chinensis var. Mairei. Biotechnol. Applied Biochem., 37: 39-43.


  • Laule, O., A. Furholz, H.S. Chang, T. Zhu, X. Wang and P.B. Heifetz et al., 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Nat. Acad. Sci. USA., 100: 6866-6871.
    Direct Link    


  • Ye, X.D., S.A. Babili, A. Kloti, J. Zhang, P. Lucca, P. Beyer and I. Potrykus, 2000. Engineering provitamin a (β-carotene) biosynthetic pathway into (caroteneoidfree) rice endosperm. Science, 287: 303-305.


  • Romer, S., P.D. Fraser, J.W. Kiano, C.A. Shipton, N. Misawa, W. Schuch and P.M. Bramley, 2000. Elevation of the provitamin a content of transgenic tomato plants. Natl. Biotechnol., 18: 666-669.


  • Mann, V., M. Harker, I. Pecker and J. Hirschberg, 2000. Metabolic engineering of astaxanthin production in tobacco flowers. Nat. Biotechnol., 18: 888-892.
    Direct Link    


  • Dannert, C.S., D. Umeno and F.H. Arnold, 2000. Molecular breeding of carotenoid biosynthetic pathways. Natl. Biotechnol., 18: 750-753.


  • Lange, B.M. and R. Croteau, 1999. Genetic engineering of essential oil production in mint. Curr. Opin. Plant Biol., 2: 139-144.


  • Martin, V.J.J., D.J. Pitera, S.T. Withers, J.D. Newman and J.D. Keasling, 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotech., 21: 796-802.


  • Fits, L.V.D. and J. Memelink, 2000. ORCA3 a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289: 295-297.


  • Jomaa, H., J. Wiesner, S. Sanderbrand, B. Altincicek and H.K. Lichtenthaler et al., 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science, 285: 1573-1576.


  • Eriksson, M.E., M. Israelsson, O. Olsson and T. Moritz, 2000. Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol., 18: 784-788.
    CrossRef    Direct Link    


  • Soriente, A., M.M.C.D. Rosa, A. Scettri, G. Sodano, M.C. Terencio, M. Paya and M.J. Alcaraz, 1999. Manoalide. Curr. Med. Chem., 6: 415-431.


  • Matthews, P.D. and E.T. Wurtzel, 2000. Metabolic engineering of carotenoid accumulation in E. coli by modulation of the isoprenoid precursor pool with expression of deoxyxylulose phosphate synthase. Applied Microbiol. Biotechnol., 53: 396-400.

  • © Science Alert. All Rights Reserved