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Chapter 8 The Methylerythritol 4-Phosphate Pathway: Regulatory Role in Plastid Isoprenoid Biosynthesis

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 31))

Summary

Plastids synthesize a variety of isoprenoid compounds that are essential for plant growth and development, like carotenoids, gibberellins, abscisic acid and the side chain of chlorophylls, plastoquinone and tocopherols. Some plastidial isoprenoids are also relevant for their biotechnological interest. The recently elucidated methylerythritol 4-phosphate (MEP) pathway provides the isopentenyl diphosphate and dimethylallyl diphosphate required for the synthesis of plastidial isoprenoids. At present, very little is known about the regulatory mechanisms underlying the control of the metabolic flux through the MEP pathway and its crosstalk with the cytosolic mevalonate (MVA) pathway. Here I summarize recent aspects related to the regulatory role of the MEP pathway in the synthesis of plastidial isoprenoids and the use of reverse genetic strategies to study the crosstalk between the MVA and the MEP pathways.

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Abbreviations

DXS:

1-deoxy-D-xylulose 5-phosphate synthase

DXR:

1-deoxy-D-xylulose 5-phosphate reductoisomerase

HDR:

1-hydroxy-2-methyl-2-(E)-butenyl diphosphate reductase

HMGR:

3-hydroxy-3-metylglutaryl coenzyme A reductase

MEP:

2-C-methyl-D-erythritol 4-phosphate

MEV:

mevinolin

MVA:

mevalonate

GGPP:

geranylgeranyl diphosphate

FSM:

fosmidomycin

References

  • Bach TJ, Boronat A, Campos N, Ferrer A and Vollack KU (1999) Mevalonate biosynthesis in plants. Crit Rev Biochem Mol Biol 34: 107–122

    Article  PubMed  CAS  Google Scholar 

  • Besumbes O, Sauret-Gueto S, Phillips MA, Imperial S, Rodriguez-Concepcion M and Boronat A (2004) Metabolic engineering of isoprenoid biosynthesis in Arabidopsis for the production of taxadiene, the first committed precursor of Taxol. Biotechnol Bioeng 88: 168–175

    Article  PubMed  CAS  Google Scholar 

  • Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat, A and Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40: 188–199

    Article  PubMed  Google Scholar 

  • Bouvier F, d’Harlingue A, Suire C, Backhaus RA and Camara B (1998) Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant Physiol 117: 1423–1431

    Article  PubMed  CAS  Google Scholar 

  • Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A and Campos N (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

    Article  PubMed  CAS  Google Scholar 

  • Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A and Rodríguez-Concepción M (2006) Enhanced flux through the methylerythritol phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol Biol 62: 683–695

    Article  PubMed  CAS  Google Scholar 

  • Chappell J, Wolf F, Proulx J, Cuellar R and Saunders C (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: 1337–1343

    PubMed  CAS  Google Scholar 

  • Croteau R, Kutchan T and Lewis N (2000). Natural products (secondary metabolites). In: Buchanan B, Gruissem W and Jones R (eds) Biochemistry and Molecular Biology of Plants. American Society of Plant Biologists, Rockville, MD, pp. 1250–1268

    Google Scholar 

  • Disch A, Hemmerlin A, Bach TJ 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

    PubMed  CAS  Google Scholar 

  • Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W and Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102: 933–938

    Article  PubMed  CAS  Google Scholar 

  • Eisenreich W, Bacher A, Arigoni D and Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61: 1401–1426

    Article  PubMed  CAS  Google Scholar 

  • Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W and Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotech J 3: 17–27

    Article  CAS  Google Scholar 

  • Estévez JM, Cantero A, Romero C, Kawaide H, Jiménez LF, Kuzuyama, T, Seto H, Kamiya Y and León P (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124: 95–103

    Article  PubMed  Google Scholar 

  • Estévez JM, Cantero A, Reindl A, Reichler S and León P (2001) 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276: 22901–22909

    Article  PubMed  Google Scholar 

  • Gondet L, Weber T, Maillot-Vernier P, Benveniste P and Bach TJ (1992) Regulatory role of microsomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase in a tobacco mutant that overproduces sterols. Biochem Biophys Res Commun 186: 888–893

    Article  PubMed  CAS  Google Scholar 

  • Hampel D, Mosandl A and Wüst M (2005) Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66: 305–311

    Article  PubMed  CAS  Google Scholar 

  • Hans J, Hause B, Strack D and Walter MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134: 614–624

    Article  PubMed  CAS  Google Scholar 

  • Harker M, Holmberg N, Clayton JC, Gibbard CL, Wallace AD, Rawlins S, Hellyer SA, Lanot A and Safford R (2003) Enhancement of seed phytosterol levels by expression of an N-terminal truncated Hevea brasiliensis (rubber tree) 3-hydroxy-3-methylglutaryl-CoA reductase. Plant Biotechnol J 1: 113–121

    Article  PubMed  CAS  Google Scholar 

  • Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M and Bach TJ (2003) Crosstalk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem 278: 26666–26676

    Article  PubMed  CAS  Google Scholar 

  • Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Türbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D and Beck E (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573–1576

    Article  PubMed  CAS  Google Scholar 

  • Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y and Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277: 45188–45194

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Suzuki M, Tang J, Nagata N, Ohyama K, Seki H, Kiuchi R, Kaneko Y, Nakazawa M, Matsui M, Matsumoto S, Yoshida S and Muranaka T (2007) LOVASTATIN INSENSITIVE 1, a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis. Plant Cell Physiol 48: 322–331

    Article  PubMed  CAS  Google Scholar 

  • Lange BM, Wildung MR, McCaskill D and Croteau R (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci USA 95: 2100–2104

    Article  PubMed  CAS  Google Scholar 

  • Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W and Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6866–6871

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Rohmer M and Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate (IPP) and isoprenoid biosynthesis in higher plants. Physiol Plant 101: 643–652

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50: 47–65

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (2010) The non-mevalonate DOXP/MEP pathway of chloroplast isoprenoid and pigment biosynthesis. In: Rebeiz CA, Benning C, Daniel H, Hoober K, Lichtenthaler HK, Portis A, Tripathy B (eds) The Chloroplast: Basics and Applications. Springer, The Netherlands, pp. 93–118

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mahmoud SS and Croteau R (2001) Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA 98: 8915–8920

    Article  PubMed  CAS  Google Scholar 

  • McGarvey DJ and Croteau R (1995) Terpenoid metabolism. Plant Cell 7: 1015–1026

    PubMed  CAS  Google Scholar 

  • Morris WL, Ducreux LJ, Hedden P, Millam S and Taylor MA (2006) Overexpression of a bacterial 1-deoxy-D-xylulose 5-phosphate synthase gene in potato tubers perturbs the isoprenoid metabolic network: implications for the control of the tuber life cycle. J Exp Bot 57: 3007–3018

    Article  PubMed  CAS  Google Scholar 

  • Muñoz-Bertomeu J, Arrillaga I, Ros R and Segura J (2006) Up-regulation of 1-deoxy-D-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142: 890–900

    Article  PubMed  Google Scholar 

  • Nagata N, Suzuki M, Yoshida S and Muranaka T (2002) Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the non-mevalonate pathwa. Planta 216: 345–350

    Article  PubMed  CAS  Google Scholar 

  • Nagegowda DA, Rhodes D and Dudareva N (2010) The role of the methyl-erythritol-phosphate pathway in rhythmic emission of volatiles. In: Rebeiz CA, Benning C, Daniel H, Hoober K, Lichtenthaler HK, Portis A, Tripathy B (eds) The Chloroplast: Basics and Applications. Springer, The Netherlands, pp. 139–153

    Chapter  Google Scholar 

  • Rodríguez-Concepción M, Ahumada I, Diez-Juez E, Sauret-Gueto S, Lois LM, Gallego F, Carretero-Paulet L, Campos N and Boronat A (2001) 1-Deoxy-D-xylulose 5-phosphate reductoisomerase and plastid isoprenoid biosynthesis during tomato fruit ripening. Plant J 27: 213–222

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Rodríguez-Concepción M, Forés O, Martínez-García JF, González V, Phillips MA, Ferrer A and Boronat A (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16: 144–156

    Article  PubMed  Google Scholar 

  • Sauret-Güeto S, Botella-Pavia P, Flores-Pérez U, Martinez-García JF, San Roman C, León P, Boronat A and Rodríguez-Concepción M (2006) Plastid cues posttranscriptionally regulate the accumulation of key enzymes of the methylerythritol phosphate pathway in Arabidopsis. Plant Physiol 141: 75–84

    Article  PubMed  Google Scholar 

  • Schwender J, Gemünden C and Lichtenthaler HK (2001) Chlorophyta exclusively use the 1-deoxyxylulose 5-phosphate/2-C-methylerythritol 4-phosphate pathway for the biosynthesis of isoprenoids. Planta 212: 416–423

    Article  PubMed  CAS  Google Scholar 

  • Stermer BA, Bianchini GM and Korth KL (1994) Regulation of HMG-CoA reductase activity in plants. J Lipid Res 35: 1133–1140

    PubMed  CAS  Google Scholar 

  • Van der Fits L and Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289: 295–297

    Article  PubMed  Google Scholar 

  • Veau B, Courtois M, Oudin A, Chenieux JC, Rideau M and Clastre M (2000) Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochim Biophys Acta 1517: 159–163

    Article  PubMed  CAS  Google Scholar 

  • Walter MH, Fester T and Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant J 21: 571–578

    Article  PubMed  CAS  Google Scholar 

  • Walter MH, Hans J and Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31: 243–254

    Article  PubMed  CAS  Google Scholar 

  • Yao H, Gong Y, Zuo K, Ling H, Qiu C, Zhang F, Wang Y, Pi Y, Liu X, Sun X and Tang K (2008) Molecular cloning, expression profiling and functional analysis of a DXR gene encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase from Camptotheca acuminata. J Plant Physiol 165: 203–213

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Work from my group has been funded by grants BIO2006-003704 from the Spanish Ministerio de Educación y Ciencia and 2005SGR00914 from the Generalitat de Catalunya

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Correspondence to Albert Boronat .

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Boronat, A. (2010). Chapter 8 The Methylerythritol 4-Phosphate Pathway: Regulatory Role in Plastid Isoprenoid Biosynthesis. In: Rebeiz, C.A., et al. The Chloroplast. Advances in Photosynthesis and Respiration, vol 31. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-8531-3_8

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