Network analysis of the MVA and MEP pathways for isoprenoid synthesis

Annual Review of Plant Biology

Volumn 64, Issue , 2013, Pages 665-700

  Vranová, Eva ^a,b   Coman, Diana ^a   Gruissem, Wilhelm ^a  

^a ETH ZURICH   (Switzerland)

^b P J AFÁRIK UNIVERSITY   (Slovakia)

Author keywords

Coexpression networks; Enzymes; Metabolite transport; Posttranslational regulation; Systems biology; Transcriptional regulation

Indexed keywords

2 C METHYLERYTHRITOL 4 PHOSPHATE; 2-C-METHYLERYTHRITOL 4-PHOSPHATE; DRUG DERIVATIVE; ERYTHRITOL; MEVALONIC ACID; SUGAR PHOSPHATE; TERPENE;

GENE REGULATORY NETWORK; METABOLISM; PLANT; PLASTID; REVIEW;

ERYTHRITOL; GENE REGULATORY NETWORKS; METABOLIC NETWORKS AND PATHWAYS; MEVALONIC ACID; PLANTS; PLASTIDS; SUGAR PHOSPHATES; TERPENES;

EID: 84877652929     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-050312-120116     Document Type: Review

References (157)

1. Ahumada I, Cairó A, Hemmerlin A, Gonzalez V, Pateraki I, et al. 2008. Characterisation of the gene family encoding acetoacetyl-CoA thiolase in Arabidopsis. Funct. Plant Biol. 35:1100-11
2. Araki N, Kusumi K, Masamoto K, Niwa Y, Iba K. 2000. Temperature-sensitive Arabidopsis mutant defective in 1-deoxy-D-xylulose 5-phosphate synthase within the plastid non-mevalonate pathway of isoprenoid biosynthesis. Physiol. Plant. 108:19-24
3. Arimura G, Garms S, Maffei M, Bossi S, Schulze B, et al. 2008. Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227:453-64
4. Balmer Y, Koller A, del Val G, ManieriW, Schurmann P, Buchanan BB. 2003. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc. Natl. Acad. Sci. USA 100:370-75
5. Bede JC,Musser RO, Felton GW, Korth KL. 2006. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol. Biol. 60:519-31
6. Berthelot K, Estevez Y, Deffieux A, Peruch F. 2012. Isopentenyl diphosphate isomerase: a checkpoint to isoprenoid biosynthesis. Biochimie 94:1621-34
7. Bick JA, Lange BM. 2003. Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch. Biochem. Biophys. 415:146-54
8. Bohlmann J, Keeling CI. 2008. Terpenoid biomaterials. Plant J. 54:656-69
9. Boucher Y, DoolittleWF. 2000. The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol. Microbiol. 37:703-16
10. Boutte Y, Grebe M. 2009. Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12:705-13
11. Bouvier F, Suire C, d'Harlingue A, Backhaus RA, Camara B. 2000. Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J. 24:241-52
12. Brodersen P, Sakvarelidze-Achard L, SchallerH,Khafif M, Schott G, et al. 2012. Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:1778-83
13. Buchanan BB, Schurmann P, Wolosiuk R, Jacquot JP. 2002. The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth. Res. 73:215-22
14. Budziszewski GJ, Lewis SP, Glover LW, Reineke J, Jones G, et al. 2001. Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning. Genetics 159:1765-78
15. Burg JS, Espenshade PJ. 2011. Regulation of HMG-CoA reductase in mammals and yeast. Prog. Lipid Res. 50:403-10
16. Burg JS, Powell DW, Chai R, Hughes AL, Link AJ, Espenshade PJ. 2008. Insig regulates HMG-CoA reductase by controlling enzyme phosphorylation in fission yeast. Cell Metab. 8:522-31
17. Caelles C, Ferrer A, Balcells L, Hegardt F, Boronat A. 1989. Isolation and structural characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Mol. Biol. 13:627-38
18. Campbell M, Hahn FM, PoulterCD, LeustekT. 1998. Analysis of the isopentenyl diphosphate isomerase gene family from Arabidopsis thaliana. Plant Mol. Biol. 36:323-28
19. Campos N, Boronat A. 1995. Targeting and topology in the membrane of plant 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Cell 7:2163-74
20. Carrie C, Murcha M, Millar A, Smith S, Whelan J. 2007. Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not to mitochondria. Plant Mol. Biol. 63:97-108
21. 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 4:1333-44
22. Closa M, Vranová E, Bortolotti C, Bigler L, Arró M, 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. 63:512-25
23. CordierH, Karst F, Bergès T. 1999. Heterologous expression in Saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol. Biol. 39:953-67
24. Cordoba E, Salmi M, León P. 2009. Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J. Exp. Bot. 60:2933-43
25. CrowellDN, Huizinga DH. 2009. Protein isoprenylation: the fat of thematter. Trends Plant Sci. 14:163-70
26. Crowell DN, Packard CE, Pierson CA, Giner JL, Downes BP, Chary SN. 2003. Identification of an allele of CLA1 associated with variegation in Arabidopsis thaliana. Physiol. Plant. 118:29-37
27. Cunillera N, ArróM, Delourme D, Karst F, Boronat A, Ferrer A. 1996. Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genes. J. Biol. Chem. 271:7774-80
28. Cunillera N, Boronat A, Ferrer A. 1997. The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 272:15381-88
29. Delourme D, Lacroute F, Karst F. 1994. Cloning of an Arabidopsis thaliana cDNA coding for farnesyl diphosphate synthase by functional complementation in yeast. Plant Mol. Biol. 26:1867-73
30. Denbow CJ, Lång S,CramerCL. 1996. TheN-terminal domain of tomato 3-hydroxy-3-methylglutaryl-CoA reductases. J. Biol. Chem. 271:9710-15
31. Disch A, Rohmer M. 1998. On the absence of the glyceraldehyde 3-phosphate/pyruvate pathway for isoprenoid biosynthesis in fungi and yeasts. FEMS Microbiol. Lett. 168:201-8
32. Disch A, Schwender J, M? uller C, Lichtenthaler HK, Rohmer M. 1998. Distribution of the mevalonate and glyceraldehyde phosphate/pyruvate pathways for isoprenoid biosynthesis in unicellular algae and the cyanobacterium Synechocystis PCC 6714. Biochem. J. 333:381-88
33. Dos Santos CV, Letousey P, Delavault P, Thalouarn P. 2003. Defense gene expression analysis of Arabidopsis thaliana parasitized by Orobanche ramosa. Phytopathology 93:451-57
34. Douglas P, Pigaglio E, Ferrer A, Halfords NG, MacKintosh C. 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. 325:101-9
35. Enjuto M, Balcells L, Campos N, Caelles C, Arro M, Boronat A. 1994. Arabidopsis thaliana contains two differentially expressed 3-hydroxy-3- methylglutaryl-CoA reductase genes, which encode microsomal forms of the enzyme. Proc. Natl. Acad. Sci. USA 91:927-31
36. Enjuto M, Lumbreras V, Marin C, Boronat A. 1995. Expression of the Arabidopsis HMG2 gene, encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase, is restricted to meristematic and floral tissues. Plant Cell 7:517-27
37. Estevez JM, Cantero A, Romero C, Kawaide H, Jimenez LF, et al. 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. 124:95-104
38. Flores-Perez Ú, Perez-Gil J, ClosaM,Wright LP, Botella-Pavia P, et al. 2010. PLEIOTROPIC REGULATORY LOCUS 1 (PRL1) integrates the regulation of sugar responses with isoprenoid metabolism in Arabidopsis. Mol. Plant 3:101-12
39. Flores-Perez Ú, Sauret-Gu? eto S, Gas E, Jarvis P, Rodriguez-Concepción M. 2008. A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20:1303-15
40. Galichet A, Gruissem W. 2003. Protein farnesylation in plants - conserved mechanisms but different targets. Curr. Opin. Plant Biol. 6:530-35
41. Gerber E, Hemmerlin A, Hartmann M, Heintz D, Hartmann MA, et al. 2009. The plastidial 2-Cmethyl-D-erythritol 4-phosphate pathway provides the isoprenyl moiety for protein geranylgeranylation in tobacco BY-2 cells. Plant Cell 21:285-300
42. Ghassemian M, Lutes J, Tepperman JM, Chang HS, Zhu T, et al. 2006. Integrative analysis of transcript and metabolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis. Arch. Biochem. Biophys. 448:45-59
43. GilMJ, CoegoA,Mauch-ManiB, Jorda L, Vera P. 2005. TheArabidopsis csb3 mutant reveals a regulatory link between salicylic acid-mediated disease resistance and the methyl-erythritol 4-phosphate pathway. Plant J. 44:155-66
44. Goldstein JL, DeBose-Boyd RA, Brown AE. 2006. Protein sensors formembrane sterols. Cell 124:35-46
45. Gu ZL, Nicolae D, Lu HHS, Li WH. 2002. Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet. 18:609-13
46. GuirimandG,Guihur A, PhillipsM,Oudin A,GlevarecG, et al. 2012. A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Mol. Biol. 79:443-59
47. Gutierrez-Nava ML, Gillmor CS, Jimenez LF, Guevara-Garcia A, León P. 2004. CHLOROPLAST BIOGENESIS genes act cell and noncell autonomously in early chloroplast development. Plant Physiol. 135:471-82
48. Hartmann M-A. 2004. Sterol metabolism and functions in higher plants. In Lipid Metabolism and Membrane Biogenesis, ed. G Daum, pp. 183-211. Berlin: Springer
49. Hemmerlin A, Harwood JL, Bach TJ. 2012. A raison d'̂etre for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog. Lipid Res. 51:95-148
50. Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Isabelle A, et al. 2003. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J. Biol. Chem. 278:26666-76
51. Herde M, Gartner K, Kollner TG, Fode B, Boland W, et al. 2008. Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20:1152-68
52. Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, et al. 2010. Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol. 153:757-72
53. Hojo M, Tasaka M, Shikanai T. 2005. Physiological requirements of the nonmevalonate pathway for photo-acclimation in Arabidopsis. Plant Biotechnol. 22:39-45
54. Hsieh F-L, Chang T-H, Ko T-P, Wang AH-J. 2011. Structure and mechanism of an Arabidopsis medium/long-chain-length prenyl pyrophosphate synthase. Plant Physiol. 155:1079-90
55. HsiehMH, Chang CY, Hsu SJ, Chen JJ. 2008. Chloroplast localization ofmethylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Mol. Biol. 66:663-73
56. Hsieh MH, Goodman HM. 2005. The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol. 138:641-53
57. HsiehMH, Goodman HM. 2006. Functional evidence for the involvement of Arabidopsis IspF homolog in the nonmevalonate pathway of plastid isoprenoid biosynthesis. Planta 223:779-84
58. InnanH,Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11:97-108
59. Ishiguro S,Nishimori Y, Yamada M, Saito H, Suzuki T, et al. 2010. The Arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl-coenzyme A synthase required for development of tapetumspecific organelles and fertility of pollen grains. Plant Cell Physiol. 51:896-911
60. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, et al. 2008. The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832-35
61. Jin H, Song Z, Nikolau BJ. 2012. Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development. Plant J. 70:1015-32
62. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, et al. 2009. Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol. Plant 2:1154-80
63. Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, et al. 2011. Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J. Exp. Bot. 62:2915-24
64. Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S. 2002. Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J. Biol. Chem. 277:45188-94
65. Kasahara H, Takei K, Ueda N, Hishiyama S, Yamaya T, et al. 2004. Distinct isoprenoid origins of cisand trans-zeatin biosyntheses in Arabidopsis. J. Biol. Chem. 279:14049-54
66. Kim CY, Zhang S. 2004. Activation of amitogen-activated protein kinase cascade inducesWRKYfamily of transcription factors and defense genes in tobacco. Plant J. 38:142-51
67. Kliebenstein DJ. 2004. Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant Cell Environ. 27:675-84
68. Kobayashi K, Suzuki M, Tang J, Nagata N, Ohyama K, et al. 2007. LOVASTATIN INSENSITIVE 1, a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis. Plant Cell Physiol. 48:322-31
69. Kovacs WJ, Olivier LM, Krisans SK. 2002. Central role of peroxisomes in isoprenoid biosynthesis. Prog. Lipid Res. 41:369-91
70. Lange BM, Croteau R. 1999. Isopentenyl diphosphate biosynthesis via a mevalonate-independent pathway: Isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. Proc. Natl. Acad. Sci. USA 96:13714-19
71. Lange BM, Ghassemian M. 2003. Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol. Biol. 51:925-48
72. Lange BM, Rujan T,MartinW, Croteau R. 2000. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. USA 97:13172-77
73. Lange BM, Wildung MR, McCaskill D, Croteau R. 1998. A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. USA 95:2100-4
74. Laule O, Furholz A, Chang H-S, Zhu T, Wang X, et al. 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100:6866-71
75. Leivar P, Antolin-Llovera M, Ferrero S, Closa M, Arró M, et al. 2011. Multilevel control of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase by protein phosphatase 2a. Plant Cell 23:1494-511
76. Leivar P, González VM, Castel S, Trelease RN, López- Iglesias C, et al. 2005. Subcellular localization of Arabidopsis 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Plant Physiol. 137:57-69
77. Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P. 2004. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 101:7475-80
78. 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
79. Lumbreras V, Campos N, Boronat A. 1995. The use of an alternative promoter in the Arabidopsis thaliana HMG1gene generates anmRNAthat encodes a novel 3-hydroxy-3-methylglutaryl coenzymeAreductase isoform with an extended N-terminal region. Plant J. 8:541-49
80. Lutke-Brinkhaus F, Liedvogel B, Kleinig H. 1984. On the biosynthesis of ubiquinones in plant mitochondria. Eur. J. Biochem. 141:537-41
81. LynchM,Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-55
82. Malkin R, Niyogi K. 2000. Photosynthesis. In Biochemistry and Molecular Biology of Plants, ed. BB Buchanan,WGruissem, RL Jones, pp. 568-628. Rockville, MD: Am. Soc. Plant Physiol
83. Mandel MA, Feldmann KA, Herrera-Estrella L, Rocha-Sosa M, Leon P. 1996. CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 9:649-58
84. Manzano D, Busquets A, Closa M, Hoyerová K, Schaller H, et al. 2006. Overexpression of farnesyl diphosphate synthase in Arabidopsis mitochondria triggers light-dependent lesion formation and alters cytokinin homeostasis. Plant Mol. Biol. 61:195-213
85. Mayzlish-Gati E, De Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, et al. 2012. Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol. 160:1329-41
86. Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET. 2011. A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst. Biol. 5:77
87. Miziorko HM. 2011. Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch. Biochem. Biophys. 505:131-43
88. Montamat F, GuillotonM, Karst F, Delrot S. 1995. Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3- methylglutaryl-coenzyme A synthase. Gene 167:197-201
89. Montiel G, Breton C, Thiersault M, Burlat V, Jay-Allemand C, Gantet P. 2007. Transcription factor Agamous-like 12 from Arabidopsis promotes tissue-like organization and alkaloid biosynthesis in Catharanthus roseus suspension cells. Metab. Eng. 9:125-32
90. Nagata N, Suzuki M, Yoshida S, Muranaka T. 2002. Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the non-mevalonate pathway. Planta 216:345-50
91. Nagegowda DA, Ramalingam S, Hemmerlin A, Bach TJ, Chye M-L. 2005. Brassica juncea HMG-CoA synthase: localization of mRNA and protein. Planta 221:844-56
92. Nieto B, Fores O, Arró M, Ferrer A. 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 70:53-59
93. Ober D. 2010. Gene duplications and the time thereafter: examples from plant secondary metabolism. Plant Biol. 12:570-77
94. Ohyama K, Suzuki M, Masuda K, Yoshida S, Muranaka T. 2007. Chemical phenotypes of the hmg1 and hmg2 mutants of Arabidopsis demonstrate the in-planta role of HMG-CoA reductase in triterpene biosynthesis. Chem. Pharm. Bull. 55:1518-21
95. Okada K, Kasahara H, Yamaguchi S, Kawaide H, Kamiya Y, et al. 2008. Genetic evidence for the role of isopentenyl diphosphate isomerases in the mevalonate pathway and plant development in Arabidopsis. Plant Cell Physiol. 49:604-16
96. Okada K, Kawaide H, Kuzuyama T, Seto H, Curtis I, Kamiya Y. 2002. Antisense and chemical suppression of the nonmevalonate pathway affects ent-kaurene biosynthesis in Arabidopsis. Planta 215:339-44
97. Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y. 2000. Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol. 122:1045-56
98. Peretó J, López-Garcia P, Moreira D. 2005. Phylogenetic analysis of eukaryotic thiolases suggests multiple proteobacterial origins. J. Mol. Evol. 61:65-74
99. Phillips MA, D'Auria JC, Gershenzon J, Pichersky E. 2008. The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 20:677-97 99a.
100. PhillipsMA, León P, Boronat A, Rodriguez-Concepción M. 2008. The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci. 13:619-23
101. Proteau PJ. 1998. Biosynthesis of phytol in the cyanobacterium Synechocystis sp. UTEX 2470: utilization of the non-mevalonate pathway. J. Nat. Prod. 61:841-43
102. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, et al. 2012. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158:1976-87
103. 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. 65:443-59
104. Reumann S. 2004. Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 135:783-800
105. Riou C, Tourte Y, Lacroute F, Karst F. 1994. Isolation and characterization of a cDNA encoding Arabidopsis thaliana mevalonate kinase by genetic complementation in yeast. Gene 148:293-97
106. Rodriguez-Concepción M. 2006. Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem. Rev. 5:1-15
107. Rodriguez-Concepción M. 2010. Supply of precursors for carotenoid biosynthesis in plants. Arch. Biochem. Biophys. 504:118-22
108. Rodriguez-Concepción M, Boronat A. 2013. Isoprenoid biosynthesis in prokaryotic organisms. In Isoprenoid Synthesis in Plants and Microorganisms, ed. TJ Bach, M Rohmer, pp. 1-16. New York: Springer
109. Rodriguez-Concepción M, Fores O, Martinez-Garcia JF, Gonzalez V, Phillips MA, et al. 2004. Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16:144-56
110. Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, et al. 2003. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc. Natl. Acad. Sci. USA 100:1586-91
111. Rohmer M, Knani M, Simonin P, Sutter B, Sahm H. 1993. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J. 295:517-24
112. Sallaud C, Rontein D, Onillon S, Jabès F, Duffe P, et al. 2009. A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301-17
113. Santner A, Calderon-Villalobos LIA, Estelle M. 2009. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5:301-7
114. Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, et al. 2008. Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol. 148:1219-28
115. Sauret-Gueto S, Botella-Pavia P, Flores-PerezU,Martinez-Garcia JF, San Roman C, et al. 2006. Plastid cues posttranscriptionally regulate the accumulation of key enzymes of the methylerythritol phosphate pathway in Arabidopsis. Plant Physiol. 141:75-84
116. Schmid M, Davison TS, Henz SR, Pape UJ, DemarM, et al. 2005. A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37:501-6
117. Schuhr CA, Radykewicz T, Sagner S, Latzel C, Zenk MH, et al. 2003. Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochem. Rev. 2:3-16
118. Schurmann P, Jacquot J. 2000. Plant thioredoxin systems revisited. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:371-400
119. Seemann M, Bui B, Wolff M, Tritsch D, Campos N, et al. 2002. Isoprenoid biosynthesis through the methylerythritol phosphate pathway: The (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (GcpE) is a [4Fe-4S] protein. Angew. Chem. Int. Ed. 41:4337-39
120. SeemannM, Tse Sum Bui B, WolffM,Miginiac-Maslow M, Rohmer M. 2006. Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG. FEBS Lett. 580:1547-52
121. Seemann M, Wegner P, Sch ?unemann V, Bui BTS, Wolff M, et al. 2005. Isoprenoid biosynthesis in chloroplasts via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (GcpE) from Arabidopsis thaliana is a [4Fe-4S] protein. J. Biol. Inorg. Chem. 10:131-37
122. Seto H, Watanabe H, Furihata K. 1996. Simultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenyl diphosphate in Streptomyces aeriouvifer. Tetrahedron Lett. 37:7979-82
123. Sever N, Yang T, BrownMS, Goldstein JL, DeBose-Boyd RA. 2003. Accelerated degradation of HMG CoA reductase mediated by binding of insig-1 to its sterol-sensing domain. Mol. Cell 11:25-33
124. Simkin A, Guirimand G, Papon N, Courdavault V, Thabet I, et al. 2011. Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234:903-14
125. Smit A, Mushegian A. 2000. Biosynthesis of isoprenoids via mevalonate in archaea: the lost pathway. Genome Res. 10:1468-84
126. Stephenson PG, Fankhauser C, Terry MJ. 2009. PIF3 is a repressor of chloroplast development. Proc. Natl. Acad. Sci. USA 106:7654-59
127. Stermer BA, Bianchini GM, Korth KL. 1994. Regulation of HMG-CoA reductase activity in plants. J. Lipid Res. 35:1133-40
128. Suzuki M, Kamide Y, Nagata N, Seki H, Ohyama K, 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. 37:750-61
129. Suzuki M, Nakagawa S, Kamide Y, Kobayashi K, Ohyama K, et al. 2009. Complete blockage of the mevalonate pathway results in male gametophyte lethality. J. Exp. Bot. 60:2055-64
130. Tang J, Kobayashi K, SuzukiM,Matsumoto S, Muranaka T. 2010. Themitochondrial PPR protein LOVASTATIN INSENSITIVE 1 plays regulatory roles in cytosolic and plastidial isoprenoid biosynthesis through RNA editing. Plant J. 61:456-66
131. Thabet I, Guirimand G, Courdavault V, Papon N, Godet S, et al. 2011. The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J. Plant Physiol. 168:2110-16
132. Tholl D, Lee S. 2011. Terpene specialized metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0143
133. Thulasiram HV, Erickson HK, Poulter CD. 2007. Chimeras of two isoprenoid synthases catalyze all four coupling reactions in isoprenoid biosynthesis. Science 316:73-76
134. Toledo-Ortiz G, Huq E, Quail PH. 2003. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749-70
135. Toledo-Ortiz G, Huq E, Rodriguez-Concepción M. 2010. Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. USA 107:11626-31
136. van der Fits L, Memelink J. 2000. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295-97
137. Vandermoten S, Haubruge É, CussonM. 2009. New insights into short-chain prenyltransferases: structural features, evolutionary history and potential for selective inhibition. Cell Mol. Life Sci. 66:3685-95
138. van Wezel GP, McDowall KJ. 2011. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat. Prod. Rep. 28:1311-33
139. Vogeli U, Chappell J. 1988. Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol. 88:1291-96
140. Vranová E, Coman D, GruissemW. 2012. Structure and dynamics of the isoprenoid pathway network. Mol. Plant 5:318-33
141. Vranová E, Hirsch-Hoffmann M, Gruissem W. 2011. AtIPD: a curated database of Arabidopsis isoprenoid pathway models and genes for isoprenoid network analysis. Plant Physiol. 156:1655-60
142. Vranová E, Inze D, Van Breusegem F. 2002. Signal transduction during oxidative stress. J. Exp. Bot. 53:1227-36
143. Walter MH, Hans J, 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. 31:243-54
144. Wang G, Dixon RA. 2009. Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc. Natl. Acad. Sci. USA 106:9914-919
145. Weber APM, Link M, Bhattacharya D. 2006. Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot. Cell 5:609-12
146. Welsch R, Maass D, Voegel T, Dellapenna D, Beyer P. 2007. Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol. 145:1073-85
147. Wilding EI, Brown JR, Bryant AP, Chalker AF, Holmes DJ, et al. 2000. Identification, evolution, and essentiality of the mevalonate pathway for isopentenyl diphosphate biosynthesis in gram-positive cocci. J. Bacteriol. 182:4319-27
148. Wille A, ZimmermannP,Vranova E, FurholzA,Laule O, et al. 2004. Sparse graphical Gaussian modeling of the isoprenoid gene network in Arabidopsis thaliana. Genome Biol. 5:R92
149. Wolff M, Seemann M, Tse Sum Bui B, Frapart Y, Tritsch D, et al. 2003. Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe-4S] protein. FEBS Lett. 541:115-20
150. Xing S, Miao J, Li S, Qin G, Tang S, et al. 2010. Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis. Cell Res. 20:688-700
151. Yang C-Q, Espenshade PJ, Wright LP, Yabe D, Gong Y, et al. 2002. Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110:489-500
152. Yang K-Y, Liu Y, Zhang S. 2001. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98:741-46
153. Yoshioka A, Miho M, Yukie H, Noriyuki D. 1996. Expression of genes for phenylalanine ammonialyase and 3-hydroxy-3-methylglutaryl CoA reductase in aged potato tubers infected with Phytophthora infestans. Plant Cell Physiol. 37:81-90
154. Zhang JZ. 2003. Evolution by gene duplication: an update. Trends Ecol. Evol. 18:292-98
155. Zhou Z, Gu J, Li YQ,Wang Y. 2012. Genome plasticity and systems evolution in Streptomyces. BMC Bioinforma. 13:S8
156. Zhu XF, Suzuki K, Okada K, Tanaka K, Nakagawa T, et al. 1997. Cloning and functional expression of a novel geranylgeranyl pyrophosphate synthase gene from Arabidopsis thaliana in Escherichia coli. Plant Cell Physiol. 38:357-61
157. Zhu XF, Suzuki K, Saito T, Okada K, Tanaka K, et al. 1997. Geranylgeranyl pyrophosphate synthase encoded by the newly isolated gene GGPS6 from Arabidopsis thaliana is localized in mitochondria. Plant Mol. Biol. 35:331-41