Metabolic engineering with plants for a sustainable biobased economy

Annual Review of Chemical and Biomolecular Engineering

Volumn 4, Issue , 2013, Pages 211-237

  Yoon, Jong Moon ^a   Zhao, Le ^a   Shanks, Jacqueline V ^a  

^a Iowa State University   (United States)

Author keywords

Biomass component; Cell wall engineering; Plant based enzyme; Platform chemical; Secondary metabolite

Indexed keywords

BIOCHEMISTRY; CELL ENGINEERING; CHEMICAL CONTAMINATION; FOOD SUPPLY; METABOLIC ENGINEERING; METABOLITES; MOLECULAR BIOLOGY; POPULATION STATISTICS;

BIOMASS COMPONENTS; BIOSYNTHESIS PATHWAYS; CELL WALLS; INTEGRATIVE ANALYSIS; NON-RENEWABLE NATURAL RESOURCES; PLATFORM CHEMICALS; SECONDARY METABOLITES; SUSTAINABLE PRODUCTION;

PLANTS (BOTANY);

CROP; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLIC ENGINEERING; METABOLISM; METHODOLOGY; PLANT; REVIEW; TRANSGENIC PLANT;

CROPS, AGRICULTURAL; METABOLIC ENGINEERING; PLANTS; PLANTS, GENETICALLY MODIFIED;

EID: 84883736817     PISSN: 19475438     EISSN: None     Source Type: Journal    
DOI: 10.1146/annurev-chembioeng-061312-103320     Document Type: Article

References (181)

1. Dep. Econ. Soc. Aff. 2011. World Population Prospects: The 2010 Revision, Highlights and Advance Tables. New York: United Nations
2. Hanson AD, Shanks JV. 2002. Plant metabolic engineering -entering the S curve. Metab. Eng. 4:1-2
3. Brautigam A, Gowik U. 2010. What can next generation sequencing do for you? Next generation sequencing as a valuable tool in plant research. Plant Biol. 12:831-41
4. Furbank RT, Tester M. 2011. Phenomics -technologies to relieve the phenotyping bottleneck. Trends Plant Sci. 16:635-44
5. Chundawat SPS, Beckham GT,HimmelME, Dale BE. 2011. Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu. Rev. Chem. Biomol. Eng. 2:121-45
6. Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD. 2012. Microbial engineering for the production of advanced biofuels. Nature 488:320-28
7. Oksman-Caldentey KM, Saito K. 2005. Integrating genomics and metabolomics for engineering plant metabolic pathways. Curr. Opin. Biotechnol. 16:174-49
8. Capell T, Christou P. 2004. Progress in plant metabolic engineering. Curr. Opin. Biotechnol. 15:148-54
9. Metzker ML. 2010. Sequencing technologies -the next generation. Nat. Rev. Genet. 11:31-46
10. Weckwerth W. 2011. Green systems biology -from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J. Proteomics 75:284-305
11. Ozsolak F, Milos PM. 2011. RNA sequencing: Advances, challenges and opportunities. Nat. Rev. Genet. 12:87-98
12. Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57-63
13. Hamilton JP, Robin Buell C. 2012. Advances in plant genome sequencing. Plant J. 70:177-90
14. Champagne A, Boutry M. 2013. Proteomics of nonmodel plant species. Proteomics 13:1-11
15. Lessard PA, Kulaveerasingam H, York GM, Strong A, Sinskey AJ. 2002. Manipulating gene expression for the metabolic engineering of plants. Metab. Eng. 4:67-79
16. Potenza C, Aleman L, Sengupta-Gopalan C. 2004. Targeting transgene expression in research, agricultural, and environmental applications: Promoters used in plant transformation. In Vitro Cell. Dev. Biol. Plant 40:1-22
17. Osakabe K, Osakabe Y, Toki S. 2010. Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc. Natl. Acad. Sci. USA 107:12034-39
18. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, et al. 2013. Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161:20-27
19. Gao H, Smith J, Yang M, Jones S, Djukanovic V, et al. 2010. Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J. 61:176-87
20. Tzfira T,Weinthal D, Marton I, Zeevi V, Zuker A, Vainstein A. 2012. Genome modifications in plant cells by custom-made restriction enzymes. Plant Biotechnol. J. 10:373-89
21. Nordhoff E, Egelhofer V, Giavalisco P, Eickhoff H, Horn M, et al. 2001. Large-gel two-dimensional electrophoresis-matrix assisted laser desorption/ionization-time of flight-mass spectrometry: An analytical challenge for studying complex protein mixtures. Electrophoresis 22:2844-55
22. Wu CC, MacCoss MJ. 2002. Shotgun proteomics: Tools for the analysis of complex biological systems. Curr. Opin. Mol. Ther. 4:242-50
23. Weckwerth W. 2008. Integration of metabolomics and proteomics in molecular plant physiology -coping with the complexity by data-dimensionality reduction. Physiol. Plant. 132:176-89
24. Kelstrup CD,YoungC,LavalleeR,Nielsen ML,Olsen JV. 2012. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole Orbitrap mass spectrometer. J. Proteome Res. 11:3487-97
25. Michalski A, Damoc E, Lange O, Denisov E, Nolting D, et al. 2012. Ultra high resolution linear ion trap Orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Mol. Cell. Proteomics 11:O111.013698
26. Trethewey RN. 2004. Metabolite profiling as an aid to metabolic engineering in plants. Curr. Opin. Plant Biol. 7:196-201
27. Plant Metab. Netw. 2012. PMN Database Content Statistics: Current PMN (7.0) Release -August 2012. Stanford: Plant Metab. Netw. http://www.plantcyc. org/release-notes/content-statistics.faces# aracyc
28. Saito K, Matsuda F. 2010. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 61:463-89
29. Mondello L, Tranchida PQ, Dugo P, Dugo G. 2008. Comprehensive two-dimensional gas chromatography-mass spectrometry: A review. Mass Spectrom. Rev. 27:101-24
30. HendricksonCL, Emmett MR. 1999. Electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Annu. Rev. Phys. Chem. 50:517-36
31. Lee YJ, Perdian DC, Song Z, Yeung ES, Nikolau BJ. 2012. Use of mass spectrometry for imaging metabolites in plants. Plant J. 70:81-95
32. Wiechert W. 2001. 13C metabolic flux analysis. Metab. Eng. 3:195-206
33. ZamboniN, Fendt SM, Ruhl M, Sauer U. 2009. 13C-based metabolic flux analysis. Nat. Protoc. 4:878-92
34. Tang Y, Pingitore F, Mukhopadhyay A, Phan R, Hazen TC, Keasling JD. 2007. Pathway confirmation and flux analysis of central metabolic pathways in Desulfovibrio vulgaris Hildenborough using gas chromatography-mass spectrometry and Fourier transform-ion cyclotron resonance mass spectrometry. J. Bacteriol. 189:940-49
35. Crown SB, Indurthi DC, Ahn WS, Choi J, Papoutsakis ET, Antoniewicz MR. 2011. Resolving the TCAcycle and pentose-phosphate pathway of Clostridium acetobutylicumATCC824: Isotopomer analysis, in vitro activities and expression analysis. Biotechnol. J. 6:300-5
36. Fendt SM, Oliveira AP, Christen S, Picotti P, Dechant RC, Sauer U. 2010. Unraveling conditiondependent networks of transcription factors that control metabolic pathway activity in yeast. Mol. Syst. Biol. 6:432
37. Gombert AK, Moreira dos Santos M, Christensen B, Nielsen J. 2001. Network identification and flux quantification in the central metabolism of Saccharomyces cerevisiae under different conditions of glucose repression. J. Bacteriol. 183:1441-51
38. Iyer VV, Sriram G, Fulton DB, Zhou R,WestgateME, Shanks JV. 2008. Metabolic fluxmaps comparing the effect of temperature on protein and oil biosynthesis in developing soybean cotyledons. Plant Cell Environ. 31:506-17
39. Alonso AP, Raymond P, Hernould M, Rondeau-Mouro C, de Graaf A, et al. 2007. A metabolic flux analysis to study the role of sucrose synthase in the regulation of the carbon partitioning in central metabolism in maize root tips. Metab. Eng. 9:419-32
40. Lonien J, Schwender J. 2009. Analysis of metabolic flux phenotypes for two Arabidopsis mutants with severe impairment in seed storage lipid synthesis. Plant Physiol. 151:1617-34
41. O'Grady J, Schwender J, Shachar-Hill Y, Morgan JA. 2012. Metabolic cartography: Experimental quantification of metabolic fluxes from isotopic labelling studies. J. Exp. Bot. 63:2293-308
42. Wiechert W, Möllney M, Petersen S, de Graaf AA. 2001. A universal framework for 13C metabolic flux analysis. Metab. Eng. 3:265-83
43. Antoniewicz MR, Kelleher JK, Stephanopoulos G. 2007. Elementary metabolite units (EMU): A novel framework for modeling isotopic distributions. Metab. Eng. 9:68-86
44. Srour O, Young JD, Eldar YC. 2011. Fluxomers: A new approach for 13C metabolic flux analysis. BMC Syst. Biol. 5:129
45. Quek L-E, Wittmann C, Nielsen L, Krömer J. 2009. OpenFLUX: Efficient modelling software for 13C-based metabolic flux analysis. Microb. Cell Factories 8:25
46. Sriram G, Fulton DB, Iyer VV, Peterson JM, Zhou R, et al. 2004. Quantification of compartmented metabolic fluxes in developing soybean embryos by employing biosynthetically directed fractional 13C labeling, two-dimensional [13C, 1H] nuclear magnetic resonance, and comprehensive isotopomer balancing. Plant Physiol. 136:3043-57
47. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, et al. 2011. A comprehensive genome-scale reconstruction of Escherichia coli metabolism -2011. Mol. Syst. Biol. 7:535
48. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, et al. 2007. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3:121
49. Reed JL, Vo TD, Schilling CH, Palsson BO. 2003. An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol. 4:R54
50. Ranganathan S, Tee TW, Chowdhury A, Zomorrodi AR, Yoon JM, et al. 2012. An integrated analytical, computational and metabolic engineering study for overproducing fatty acids in Escherichia coli. Metab. Eng. 14:687-704
51. Ranganathan S, Suthers PF, Maranas CD. 2010. OptForce: An optimization procedure for identifying all genetic manipulations leading to targeted overproductions. PLoS Comput. Biol. 6:e1000744
52. Poolman MG, Miguet L, Sweetlove LJ, Fell DA. 2009. A genome-scale metabolic model of Arabidopsis and some of its properties. Plant Physiol. 151:1570-81
53. Gomes deOliveira Dal'Molin C, Quek LE, PalfreymanRW,Brumbley SM, NielsenLK. 2010. AraGEM, a genome-scale reconstruction of the primary metabolic network in Arabidopsis. Plant Physiol. 152:579-89
54. Grafahrend-Belau E, Schreiber F, KoschutzkiD, Junker BH. 2009. Flux balance analysis of barley seeds: A computational approach to study systemic properties of central metabolism. Plant Physiol. 149:585-98
55. Hay J, Schwender J. 2011. Computational analysis of storage synthesis in developing Brassica napus L. (oilseed rape) embryos: Flux variability analysis in relation to 13C metabolic flux analysis. Plant J. 67:513-25
56. Gomes de Oliveira Dal'Molin C, Quek L-E, Palfreyman RW, Brumbley SM, Nielsen LK. 2010. C4GEM, a genome-scale metabolic model to study C4 plant metabolism. Plant Physiol. 154:1871-85
57. Saha R, Suthers PF, Maranas CD. 2011. Zea mays iRS1563: A comprehensive genome-scale metabolic reconstruction of maize metabolism. PLoS One 6:e21784
58. Xu P, Ranganathan S, Fowler ZL, Maranas CD, Koffas MAG. 2011. Genome-scale metabolic network modeling results in minimal interventions that cooperatively force carbon flux towards malonyl-CoA. Metab. Eng. 13:578-87
59. Collakova E, Yen JY, Senger RS. 2012. Are we ready for genome-scale modeling in plants? Plant Sci. 191-192:53-70
60. Seaver SM, Henry CS, Hanson AD. 2012. Frontiers in metabolic reconstruction and modeling of plant genomes. J. Exp. Bot. 63:2247-58
61. Fernie AR,Willmitzer L, Trethewey RN. 2002. Sucrose to starch: A transition in molecular plant physiology. Trends Plant Sci. 7:35-41
62. Comparot-Moss S, Denyer K. 2009. The evolution of the starch biosynthetic pathway in cereals and other grasses. J. Exp. Bot. 60:2481-92
63. Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM. 1992. Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science 258:287-92
64. Sweetlove LJ, Burrell MM, ap Rees T. 1996. Characterization of transgenic potato (Solanum tuberosum) tubers with increased ADPglucose pyrophosphorylase. Biochem. J. 320:487-92
65. Ihemere U, Arias-Garzon D, Lawrence S, Sayre R. 2006. Genetic modification of cassava for enhanced starch production. Plant Biotechnol. J. 4:453-65
66. Wang Z, Chen X, Wang J, Liu T, Liu Y, et al. 2007. Increasing maize seed weight by enhancing the cytoplasmic ADP-glucose pyrophosphorylase activity in transgenic maize plants. Plant Cell Tissue Organ Cult. 88:83-92
67. Geigenberger P, Stamme C, Tjaden J, Schulz A, Quick PW, et al. 2001. Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiol. 125:1667-78
68. Zhang L, Häusler RE, Greiten C, HajirezaeiM-R, Haferkamp I, et al. 2008. Overriding the co-limiting import of carbon and energy into tuber amyloplasts increases the starch content and yield of transgenic potato plants. Plant Biotechnol. J. 6:453-64
69. Zeeman SC, Kossmann J, Smith AM. 2010. Starch: Its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61:209-34
70. Weise SE, Aung K, Jarou ZJ, Mehrshahi P, Li Z, et al. 2012. Engineering starch accumulation by manipulation of phosphate metabolism of starch. Plant Biotechnol. J. 10:545-54
71. Herman EM, Larkins BA. 1999. Protein storage bodies and vacuoles. Plant Cell 11:601-13
72. Galili G, Hofgen R. 2002. Metabolic engineering of amino acids and storage proteins in plants. Metab. Eng. 4:3-11
73. Iyer VV. 2006. Carbon-13 metabolic flux analysis of soybean central carbon metabolism: Response to temperature and genotype effects. PhD thesis. Iowa State Univ. 217 pp.
74. Zhu X,Galili G. 2003. Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15:845-53
75. Tzin V, Malitsky S, Aharoni A, Galili G. 2009. Expression of a bacterial bi-functional chorismate mutase/ prephenate dehydratase modulates primary and secondary metabolism associated with aromatic amino acids in Arabidopsis. Plant J. 60:156-67
76. Qi QG, Huang JT, Crowley J, Ruschke L, Goldman BS, et al. 2011. Metabolically engineered soybean seed with enhanced threonine levels: Biochemical characterization and seed-specific expression of lysineinsensitive variants of aspartate kinases from the enteric bacterium Xenorhabdus bovienii. Plant Biotechnol. J. 9:193-204
77. Ishihara A, Asada Y, Takahashi Y, Yabe N, Komeda Y, et al. 2006. Metabolic changes in Arabidopsis thaliana expressing the feedback-resistant anthranilate synthase αsubunit gene OASA1D. Phytochemistry 67:2349-62
78. Matsuda F, Yamada T, Miyazawa H, Miyagawa H, Wakasa K. 2005. Characterization of tryptophanoverproducing potato transgenic for a mutant rice anthranilate synthase α-subunit gene (OASA1D). Planta 222:535-45
79. Carlsson AS, Yilmaz JL, Green AG, Stymne S, Hofvander P. 2011. Replacing fossil oil with fresh oil -With what and for what? Eur. J. Lipid Sci. Technol. 113:812-31
80. Thelen JJ, Ohlrogge JB. 2002. Metabolic engineering of fatty acid biosynthesis in plants. Metab. Eng. 4:12-21
81. Weselake RJ, Taylor DC, Rahman MH, Shah S, Laroche A, et al. 2009. Increasing the flow of carbon into seed oil. Biotechnol. Adv. 27:866-78
82. Vigeolas H, Geigenberger P. 2004. Increased levels of glycerol-3-phosphate lead to a stimulation of flux into triacylglycerol synthesis after supplying glycerol to developing seeds of Brassica napus L. in planta. Planta 219:827-35
83. Vigeolas H, Waldeck P, Zank T, Geigenberger P. 2007. Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol. J. 5:431-41
84. Perry HJ, Bligny R, Gout E, Harwood JL. 1999. Changes in Kennedy pathway intermediates associated with increased triacylglycerol synthesis in oil-seed rape. Phytochemistry 52:799-804
85. Taylor DC, Zhang Y, Kumar A, Francis T, Giblin EM, et al. 2009. Molecular modification of triacylglycerol accumulation by over-expression of DGAT1 to produce canola with increased seed oil content under field conditions. Botany 87:533-43
86. Zheng P, AllenWB, Roesler K,Williams ME, Zhang S, et al. 2008. A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat. Genet. 40:367-72
87. Marillia EF, Micallef BJ, Micallef M, Weninger A, Pedersen KK, et al. 2003. Biochemical and physiological studies of Arabidopsis thaliana transgenic lines with repressed expression of the mitochondrial pyruvate dehydrogenase kinase. J. Exp. Bot. 54:259-70
88. Schwender J,Goffman F, Ohlrogge JB, Shachar-Hill Y. 2004. Rubisco without theCalvin cycle improves the carbon efficiency of developing green seeds. Nature 432:779-82
89. Mendoza MS, Dubreucq B, Miquel M, Caboche M, Lepiniec L. 2005. LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 579:4666-70
90. Andrianov V, Borisjuk N, Pogrebnyak N, Brinker A, Dixon J, et al. 2010. Tobacco as a production platform for biofuel: Overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnol. J. 8:277-87
91. Pauly M, Keegstra K. 2008. Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J. 54:559-68
92. Li H, Cann AF, Liao JC. 2010. Biofuels: Biomolecular engineering fundamentals and advances. Annu. Rev. Chem. Biomol. Eng. 1:19-36
93. Perrin R,Wilkerson C, Keegstra K. 2001. Golgi enzymes that synthesize plant cell wall polysaccharides: Finding and evaluating candidates in the genomic era. Plant Mol. Biol. 47:115-30
94. Coleman HD, Yan J, Mansfield SD. 2009. Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc. Natl. Acad. Sci. USA 106:13118-23
95. Canam T, Park JY, Yu KY, Campbell MM, Ellis DD, Mansfield SD. 2006. Varied growth, biomass and cellulose content in tobacco expressing yeast-derived invertases. Planta 224:1315-27
96. Coleman HD, Ellis DD, Gilbert M, Mansfield SD. 2006. Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnol. J. 4:87-101
97. Yang JM, Chen F, Yu O, Beachy RN. 2011. Controlled silencing of 4-coumarate:CoA ligase alters lignocellulose composition without affecting stem growth. Plant Physiol. Biochem. 49:103-9
98. Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, et al. 1999. Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat. Biotechnol. 17:808-12
99. Kajita S, Hishiyama S,Tomimura Y,Katayama Y, Omori S. 1997. Structural characterization ofmodified lignin in transgenic tobacco plants in which the activity of 4-coumarate:coenzyme A ligase is depressed. Plant Physiol. 114:871-79
100. Wagner A, Donaldson L, Kim H, Phillips L, Flint H, et al. 2009. Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol. 149:370-83
101. Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annu. Rev. Plant Biol. 54:519-46
102. Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, et al. 2001. Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. Plant J. 28:257-70
103. Hoenicka H, Lautner S, Klingberg A, Koch G, El-Sherif F, et al. 2012. Influence of over-expression of the FLOWERING PROMOTING FACTOR 1 gene (FPF1) from Arabidopsis on wood formation in hybrid poplar (Populus tremula L.×P. tremuloides Michx.). Planta 235:359-73
104. Sainz MB. 2009. Commercial cellulosic ethanol: The role of plant-expressed enzymes. In Vitro Cell. Dev. Biol. Plant 45:314-29
105. Montalvo-Rodriguez R,Haseltine C, Huess-LaRossa K, Clemente T, Soto J, et al. 2000. Autohydrolysis of plant polysaccharides using transgenic hyperthermophilic enzymes. Biotechnol. Bioeng. 70:151-59
106. Santa-Maria MC, Yencho CG, Haigler CH, Thompson WF, Kelly RM, Sosinski B. 2011. Starch selfprocessing in transgenic sweet potato roots expressing a hyperthermophilic α-amylase. Biotechnol. Prog. 27:351-59
107. Collins T, Gerday C, Feller G. 2005. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev. 29:3-23
108. Kimura T, Mizutani T, Tanaka T, Koyama T, Sakka K, Ohmiya K. 2003. Molecular breeding of transgenic rice expressing a xylanase domain of the xynA gene from Clostridium thermocellum. Appl. Microbiol. Biotechnol. 62:374-79
109. Patel M, Johnson JS, Brettell RIS, Jacobsen J, Xue GP. 2000. Transgenic barley expressing a fungal xylanase gene in the endosperm of the developing grains. Mol. Breed. 6:113-23
110. Dudareva N, Pichersky E. 2008. Metabolic engineering of plant volatiles. Curr. Opin. Biotechnol. 19:181-89
111. Oksman-Caldentey KM, Inze D, Oresic M. 2004. Connecting genes to metabolites by a systems biology approach. Proc. Natl. Acad. Sci. USA 101:9949-50
112. Hughes EH, Shanks JV. 2002. Metabolic engineering of plants for alkaloid production. Metab. Eng. 4:41-48
113. Marasco E, Schmidt-Dannert C. 2007. Biosynthesis of plant natural products and characterization of plant biosynthetic pathways in recombinant microorganisms. In Applications of PlantMetabolic Engineering, ed. R Verpoorte, AWAlfermann, TS Johnson, pp. 1-43. Netherlands: Springer
114. Ziegler J, Facchini PJ. 2008. Alkaloid biosynthesis: Metabolism and trafficking. Annu. Rev. Plant Biol. 59:735-69
115. Shanks JV. 2005. Phytochemical engineering: Combining chemical reaction engineering with plant science. AIChE J. 51:2-7
116. Morgan JA, Shanks JV. 2000. Determination ofmetabolic rate-limitations by precursor feeding in Catharanthus roseus hairy root cultures. J. Biotechnol. 79:137-45
117. Canel C, Lopes-Cardoso MI, Whitmer S, Van Der Fits L, Pasquali G, et al. 1998. Effects of overexpression of strictosidine synthase and tryptophan decarboxylase on alkaloid production by cell cultures of Catharanthus roseus. Planta 205:414-19
118. Hughes EH, Hong S-B, Gibson SI, Shanks JV, San KY. 2004. Expression of a feedback-resistant anthranilate synthase in Catharanthus roseus hairy roots provides evidence for tight regulation of terpenoid indole alkaloid levels. Biotechnol. Bioeng. 86:718-27
119. Ayora-Talavera T, Chappell J, Lozoya-Gloria E, Loyola-Vargas VM. 2002. Overexpression in Catharanthus roseus hairy roots of a truncated hamster 3-hydroxy-3-methylglutaryl-CoA reductase gene. Appl. Biochem. Biotechnol. 97:135-45
120. Peebles CAM, Sander GW, Hughes EH, Peacock R, Shanks JV, San KY. 2011. The expression of 1-deoxy-D-xylulose synthase and geraniol-10-hydroxylase or anthranilate synthase increases terpenoid indole alkaloid accumulation in Catharanthus roseus hairy roots. Metab. Eng. 13:234-40
121. Peebles CAM,Hughes EH, Shanks JV, San K-Y. 2009. Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metab. Eng. 11:76-86
122. Van Der Fits L, Memelink J. 2000. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295-97
123. Van Der Fits L, Zhang H, Menke FLH, Deneka M, Memelink J. 2000. A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway. PlantMol. Biol. 44:675-85
124. Chatel G, Montiel G, Pré M, Memelink J, Thiersault M, et al. 2003. CrMYC1, a Catharanthus roseus elicitor-and jasmonate-responsive bHLH transcription factor that binds the G-box element of the strictosidine synthase gene promoter. J. Exp. Bot. 54:2587-88
125. Zhang HT, Hedhili S, Montiel G, Zhang YX, Chatel G, et al. 2011. The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of theORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. Plant J. 67:61-71
126. Suttipanta N, Pattanaik S, Kulshrestha M, Patra B, Singh SK, Yuan L. 2011. The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol. 157:2081-93
127. Suttipanta N. 2011. Characterization of G10H promoter and isolation of WRKY transcription factors involved in Catharanthus terpenoid indole alkaloid biosynthesis pathway. PhD dissertation. Univ. Kentucky
128. Sibéril Y, Benhamron S, Memelink J, Giglioli-Guivarc'h N, Thiersault M, et al. 2001. Catharanthus roseus G-box binding factors 1 and 2 act as repressors of strictosidine synthase gene expression in cell cultures. Plant Mol. Biol. 45:477-88
129. Pauw B, Hilliou FAO, Martin VS, Chatel G, de Wolf CJF, et al. 2004. Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. J. Biol. Chem. 279:52940-48
130. Bringi V, Kadkade PG, Roach BL. 2007. US Patent No. 7264951B1
131. Runguphan W, O'Connor SE. 2009. Metabolic reprogramming of periwinkle plant culture. Nat. Chem. Biol. 5:151-53
132. Runguphan W,QuXD,O'Connor SE. 2010. Integrating carbon-halogen bond formation into medicinal plant metabolism. Nature 468:461-64
133. Wang YC, Zhang HX, Zhao B, Yuan XF. 2001. Improved growth of Artemisia annua L hairy roots and artemisinin production under red light conditions. Biotechnol. Lett. 23:1971-73
134. Wang JW, Tan RX. 2002. Artemisinin production in Artemisia annua hairy root cultures with improved growth by altering the nitrogen source in the medium. Biotechnol. Lett. 24:1153-56
135. Weathers PJ, Bunk G, McCoy MC. 2005. The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell. Dev. Biol. Plant 41:47-53
136. Aquil S, Husaini AM, Abdin MZ, Rather GM. 2009. Overexpression of the HMG-CoA reductase gene leads to enhanced artemisinin biosynthesis in transgenic Artemisia annua plants. Planta Med. 75:1453-58
137. Chen D-H, Ye H-C, Li G-F. 2000. Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci. 155:179-85
138. Han JL, Liu BY, Ye HC, Wang H, Li ZQ, Li GF. 2006. Effects of overexpression of the endogenous farnesyl diphosphate synthase on the artemisinin content in Artemisia annua L. J. Integr. Plant Biol. 48:482-87
139. Ma CF, Wang HH, Lu X, Wang H, Xu GW, Liu BY. 2009. Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry. Metabolomics 5:497-506
140. Alam P, Abdin MZ. 2011. Over-expression of HMG-CoA reductase and amorpha-4,11-diene synthase genes in Artemisia annua L. and its influence on artemisinin content. Plant Cell Rep. 30:1919-28
141. Zhang L, Jing F, Li F, Li M, Wang Y, et al. 2009. Development of transgenic Artemisia annua (Chinese wormwood) plants with an enhanced content of artemisinin, an effective anti-malarial drug, by hairpin-RNA-mediated gene silencing. Biotechnol. Appl. Biochem. 52:199-207
142. Ma DM, Pu GB, Lei CY, Ma LQ, Wang HH, et al. 2009. Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the amorpha-4,11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Physiol. 50:2146-61
143. Westfall PJ, Pitera DJ, Lenihan JR, Eng D, Woolard FX, et al. 2012. Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin. Proc. Natl. Acad. Sci. USA 109(3):E111-18
144. Heinstein PF, Chang CJ. 1994. Taxol. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:663-74
145. Besumbes O, Sauret-Güeto S, Phillips MA, Imperial S, Rodŕiguez-Concepci ́on M, Boronat A. 2004. Metabolic engineering of isoprenoid biosynthesis in Arabidopsis for the production of taxadiene, the first committed precursor of Taxol. Biotechnol. Bioeng. 88:168-75
146. Kovacs K, Zhang L, Linforth R, Whittaker B, Hayes C, Fray R. 2007. Redirection of carotenoid metabolism for the efficient production of taxadiene [taxa-4(5),11(12)-diene] in transgenic tomato fruit. Transgenic Res. 16:121-26
147. Roberts S. 2007. Production and engineering of terpenoids in plant cell culture. Nat. Chem. Biol. 3:387-95
148. Ketchum REB, Wherland L, Croteau RB. 2007. Stable transformation and long-term maintenance of transgenic Taxus cell suspension cultures. Plant Cell Rep. 26:1025-33
149. Vongpaseuth K, Nims E, Amand MS, Walker EL, Roberts SC. 2007. Development of a particle bombardment-mediated transient transformation system for Taxus spp. cells in culture. Biotechnol. Prog. 23:1180-85
150. Ajikumar PK, Xiao W-H, Tyo KEJ, Wang Y, Simeon F, et al. 2010. Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70-74
151. Cantu DC, Chen YF, Reilly PJ. 2010. Thioesterases: A new perspective based on their primary and tertiary structures. Protein Sci. 19:1281-95
152. Jing F, Cantu D, Tvaruzkova J, Chipman J, Nikolau B, et al. 2011. Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem. 12:44
153. Cantu DC, Chen YF, Lemons ML, Reilly PJ. 2011. ThYme: A database for thioester-active enzymes. Nucleic Acids Res. 39:D342-D6
154. Zhang XJ, Li M, Agrawal A, San K-Y. 2011. Efficient free fatty acid production in Escherichia coli using plant acyl-ACP thioesterases. Metab. Eng. 13:713-22
155. Li M, Zhang XJ, Agrawal A, San K-Y. 2012. Effect of acetate formation pathway and long chain fatty acid CoA-ligase on the free fatty acid production in E. coli expressing acy-ACP thioesterase from Ricinus communis. Metab. Eng. 14:380-87
156. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21:796-802
157. TsurutaH, Paddon CJ, Eng D, Lenihan JR, Horning T, et al. 2009. High-level production of amorpha-4,11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS One 4:e4489
158. ChangMC, Eachus RA,Trieu W, Ro DK,Keasling JD. 2007. Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nat. Chem. Biol. 3:274-77
159. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, et al. 2006. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940-43
160. Ajikumar PK, Xiao W-H, Tyo KEJ, Wang Y, Simeon F, et al. 2010. Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70-74
161. DeJong JM, Liu Y, Bollon AP, Long RM, Jennewein S, et al. 2006. Genetic engineering of taxol biosynthetic genes in Saccharomyces cerevisiae. Biotechnol. Bioeng. 93:212-24
162. Hong SB, Peebles CAM, Shanks JV, San KY, Gibson SI. 2006. Expression of the Arabidopsis feedbackinsensitive anthranilate synthase holoenzyme and tryptophan decarboxylase genes in Catharanthus roseus hairy roots. J. Biotechnol. 122:28-38
163. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY. 2004. Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab. Eng. 6:268-76
164. SanderGW.2009. Quantitative analysis of metabolic pathways in Catharanthus roseus hairy rootsmetabolically engineered for terpenoid indole alkaloid overproduction. PhD dissertation. Iowa State Univ
165. Magnotta M, Murata J, Chen JX, De Luca V. 2007. Expression of deacetylvindoline-4-Oacetyltransferase in Catharanthus roseus hairy roots. Phytochemistry 68:1922-31
166. Noe W, Mollenschott C, Berlin J. 1984. Tryptophan decarboxylase from Catharanthus roseus cell suspension cultures: Purification, molecular and kinetic data of the homogenous protein. Plant Mol. Biol. 3:281-88
167. McKnight TD, Roessner CA,DevaguptaR, Scott AI, Nessler CL. 1990. Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus. Nucleic Acids Res. 18:4939
168. Maldonado-Mendoza IE, Burnett RJ, Nessler CL. 1992. Nucleotide sequence of a cDNA-encoding 3-hydroxy-3-methylglutaryl coenzyme a reductase from Catharanthus roseus. Plant Physiol. 100:1613-14
169. Meijer AH, Dewaal A, Verpoorte R. 1993. Purification of the cytochrome-P-450 enzyme geraniol 10-hydroxylase from cell cultures of Catharanthus roseus. J. Chromatogr. 635:237-49
170. DethierM, Deluca V. 1993. Partial purification of an N-methyltransferase involved in vindoline biosynthesis in Catharanthus roseus. Phytochemistry 32:673-78
171. St-Pierre B, De Luca V. 1995. A cytochrome-P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol. 109:131-39
172. Vazquez-Flota F,De Carolis E, Alarco AM,De Luca V. 1997. Molecular cloning and characterization of desacetoxyvindoline-4-hydroxylase, a 2-oxoglutarate dependent dioxygenase involved in the biosynthesis of vindoline in Catharanthus roseus (L) G. Don. Plant Mol. Biol. 34:935-48
173. St-Pierre B, Laflamme P, Alarco A-M, De Luca V. 1998. The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. Plant J. 14:703-13
174. Chahed K, Oudin A, Guivarc'h N, Hamdi S, Chenieux JC, et al. 2000. 1-Deoxy-D-xylulose 5-phosphate synthase from periwinkle: CDNAidentification and induced gene expression in terpenoid indole alkaloidproducing cells. Plant Physiol. Biochem. 38:559-66
175. Collu G, Unver N, Peltenburg-Looman AMG, Van Der Heijden R, Verpoorte R, Memelink J. 2001. Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett. 508:215-20
176. LevacD,Murata J,Kim WS,De LucaV. 2008. Application of carborundum abrasion for investigating the leaf epidermis: Molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase. Plant J. 53:225-36
177. Geerlings A, Ibañez MML, Memelink J, Van Der Heijden R, Verpoorte R. 2000. Molecular cloning and analysis of strictosidine β-D-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J. Biol. Chem. 275:3051-56
178. Laflamme P, St-Pierre B, De Luca V. 2001. Molecular and biochemical analysis of a Madagascar periwinkle root-specific minovincinine-19-hydroxy-O- acetyltransferase. Plant Physiol. 125:189-98
179. Rodriguez S,Compagnon V, CrouchNP, St-Pierre B, De LucaV. 2003. Jasmonate-induced epoxidation of tabersonine by a cytochrome P-450 in hairy root cultures of Catharanthus roseus. Phytochemistry 64:401-9
180. Costa MMR, Hilliou F, Duarte P, Pereira LG, Almeida I, et al. 2008. Molecular cloning and characterization of a vacuolar class III peroxidase involved in themetabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiol. 146:403-17
181. Giddings LA, Liscombe DK, Hamilton JP, Childs KL, DellaPenna D, et al. 2011. A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. J. Biol. Chem. 286:16751-57