Biosynthesis of Plant Isoprenoids: Perspectives for Microbial Engineering
Abstract
Isoprenoids are a large and highly diverse group of natural products with many functions in plant primary and secondary metabolism. Isoprenoids are synthesized from common prenyl diphosphate precursors through the action of terpene synthases and terpene-modifying enzymes such as cytochrome P450 monooxygenases. Many isoprenoids have important applications in areas such as human health and nutrition, and much effort has been directed toward their production in microbial hosts. However, many hurdles must be overcome in the elucidation and functional microbial expression of the genes responsible for biosynthesis of an isoprenoid of interest. Here, we review investigations into isoprenoid function and gene discovery in plants as well as the latest advances in isoprenoid pathway engineering in both plant and microbial hosts.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
To date, terpene accumulation for fuels has not been a large focus of algal biology, since many terpenes and derivatives have properties that make them more valuable for other uses.
“To date, terpene accumulation for fuels has not been a large focus of algal biology, since many terpenes and terpene derivatives have properties that make them more valuable for other uses, such as flavor, fragrances and antibiotics [164,165]”
From Biofuels from algae: Challenges and potential (2010) · cites this paper as [165]
Cites
Production of the antimalarial drug precursor artemisinic acid in engineered yeast
Ro, D.-K., Paradise, E. M., Ouellet, M., Fisher, K. J., Newman, K. L., Ndungu, J. M., Ho, K. A., Eachus, R. A., Ham, T. S., Kirby, J., et al. (2006) · Nature · doi:10.1038/nature04640 · Cited by 2,805 · see citing works
Self-citationEngineering the Provitamin A (β-Carotene) Biosynthetic Pathway into (Carotenoid-Free) Rice Endosperm
Ye, X., Al‐Babili, S., Klöti, A., Zhang, J., Lucca, P., Beyer, P., & Potrykus, I. (2000) · Science · doi:10.1126/science.287.5451.303 · Cited by 2,270 · see citing works
The function of terpene natural products in the natural world
Gershenzon, J., & Dudareva, N. (2007) · Nature Chemical Biology · doi:10.1038/nchembio.2007.5 · Cited by 2,161 · see citing works
Engineering a mevalonate pathway in Escherichia coli for production of terpenoids
Martin, V. J. J., Pitera, D. J., Withers, S. T., Newman, J. D., & Keasling, J. D. (2003) · Nature Biotechnology · doi:10.1038/nbt833 · Cited by 1,720 · see citing works
Self-citationImproving the nutritional value of Golden Rice through increased pro-vitamin A content
Paine, J. A., Shipton, C. A., Chaggar, S., Howells, R. M., Kennedy, M. J., Vernon, G., Wright, S. Y., Hinchliffe, E., Adams, J. L., Silverstone, A. L., et al. (2005) · Nature Biotechnology · doi:10.1038/nbt1082 · Cited by 1,457 · see citing works
The influence of natural products upon drug discovery (Antiquity to late 1999)
Newman, D. J., Cragg, G. M., & Snader, K. M. (2000) · Natural Product Reports · doi:10.1039/a902202c · Cited by 1,293 · see citing works
Cytochromes P450 as versatile biocatalysts
Bernhardt, R. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.01.026 · Cited by 888 · see citing works
Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes
Lange, B. M., Rujan, T., Martin, W., & Croteau, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240454797 · Cited by 881 · see citing works
Crystal Structure of Hemoprotein Domain of P450BM-3, a Prototype for Microsomal P450's
Ravichandran, K. G., Boddupalli, S. S., Hasermann, C. A., Peterson, J. A., & Deisenhofer, J. (1993) · Science · doi:10.1126/science.8342039 · Cited by 876 · see citing works
The 2.6-A crystal structure of Pseudomonas putida cytochrome P-450.
Poulos, T. L., Finzel, B. C., GUNSALUS, I. C., Wagner, G. C., & Kraut, J. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36209-9 · Cited by 826 · see citing works
Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective
Pichersky, E., & Gang, D. R. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01741-6 · Cited by 809 · see citing works
Outdoor cultivation of microalgae for carotenoid production: Current state and perspectives
Del Campo, J. A., García-González, M., & Guerrero, M. G. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-0844-9 · Cited by 739 · see citing works
Biosynthesis of isoprenoids via the non-mevalonate pathway
Eisenreich, W., Bacher, A., Arigoni, D., & Rohdich, F. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-3381-z · Cited by 668 · see citing works
Estévez, J. M., Cantero, A., Reindl, A., Reichler, S. A., & León, P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100854200 · Cited by 665 · see citing works
Artemisinin-Based Combination Treatment of Falciparum Malaria
Nosten, F. H., & White, N. J. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.77.181 · Cited by 663 · see citing works
Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants[W]
Aharoni, A., Giri, A. P., Deuerlein, S., Griepink, F. C., de Kogel, W. J., Verstappen, F. W. A., Verhoeven, H. A., Jongsma, M. A., Schwab, W. G., & Bouwmeester, H. J. (2003) · The Plant Cell · doi:10.1105/tpc.016253 · Cited by 543 · see citing works
Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes
Pfleger, B. F., Pitera, D. J., Smolke, C. D., & Keasling, J. D. (2006) · Nature Biotechnology · doi:10.1038/nbt1226 · Cited by 535 · see citing works
Self-citationSchuler, M. A., & Werck‐Reichhart, D. (2003) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.54.031902.134840 · Cited by 517 · see citing works
Biogenesis, molecular regulation and function of plant isoprenoids.
Bouvier, F., Rahier, A., & Camara, B. (2005) · Progress in Lipid Research · doi:10.1016/j.plipres.2005.09.003 · Cited by 498 · see citing works
Compromised disease resistance in saponin-deficient plants
Papadopoulou, K. Κ., Melton, R. E., Leggett, M., Daniels, M. J., & Osbourn, A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12923 · Cited by 466 · see citing works
Global transcription machinery engineering: A new approach for improving cellular phenotype
Alper, H. S., & Stephanopoulos, G. N. (2007) · Metabolic Engineering · doi:10.1016/j.ymben.2006.12.002 · Cited by 448 · see citing works
Terpenoids: Opportunities for Biosynthesis of Natural Product Drugs Using Engineered Microorganisms
Ajikumar, P. K., Tyo, K. E. J., Carlsen, S., Mucha, O., Too, H., & Stephanopoulos, G. N. (2008) · Molecular Pharmaceutics · doi:10.1021/mp700151b · Cited by 445 · see citing works
Harnessing plant trichome biochemistry for the production of useful compounds
Schilmiller, A. L., Last, R. L., & Pichersky, E. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03432.x · Cited by 439 · see citing works
Designed divergent evolution of enzyme function
Yoshikuni, Y., Ferrin, T. E., & Keasling, J. D. (2006) · Nature · doi:10.1038/nature04607 · Cited by 438 · see citing works
Self-citationMahmoud, S. S., & Croteau, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141237298 · Cited by 435 · see citing works
Alper, H. S., Miyaoku, K., & Stephanopoulos, G. N. (2005) · Nature Biotechnology · doi:10.1038/nbt1083 · Cited by 433 · see citing works
Martin, D. M., Fäldt, J., & Bohlmann, J. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.042028 · Cited by 414 · see citing works
Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants
Wu, S., Schalk, M., Clark, A., et al. (2006) · Nature Biotechnology · doi:10.1038/nbt1251 · Cited by 409 · see citing works
Synthetic Biology for Synthetic Chemistry
Keasling, J. D. (2008) · ACS Chemical Biology · doi:10.1021/cb7002434 · Cited by 409 · see citing works
Self-citationEngels, B., Dahm, P., & Jennewein, S. (2008) · Metabolic Engineering · doi:10.1016/j.ymben.2008.03.001 · Cited by 380 · see citing works
Production and engineering of terpenoids in plant cell culture
Roberts, S. C. (2007) · Nature Chemical Biology · doi:10.1038/nchembio.2007.8 · Cited by 372 · see citing works
Engineering Escherichia coli for production of functionalized terpenoids using plant P450s
Chang, M. C. Y., Eachus, R. A., Trieu, W., Ro, D.-K., & Keasling, J. D. (2007) · Nature Chemical Biology · doi:10.1038/nchembio875 · Cited by 364 · see citing works
Self-citationShiba, Y., Paradise, E. M., Kirby, J., Ro, D., & Keasling, J. D. (2006) · Metabolic Engineering · doi:10.1016/j.ymben.2006.10.005 · Cited by 354 · see citing works
Self-citationChappell, J., Wolf, F., Proulx, J., Cuellar, R., & Saunders, C. (1995) · Plant Physiology · doi:10.1104/pp.109.4.1337 · Cited by 335 · see citing works
(−)-Menthol biosynthesis and molecular genetics
Croteau, R., Davis, E. M., Ringer, K. L., et al. (2005) · Die Naturwissenschaften · doi:10.1007/s00114-005-0055-0 · Cited by 335 · see citing works
Neem—An Omnipotent Plant: A Retrospection
Brahmachari, G. (2004) · ChemBioChem · doi:10.1002/cbic.200300749 · Cited by 328 · see citing works
Rubio, F. C., Fern�ndez, F. G. A., P�rez, J. A. S., García-Camacho, F., & Grima, E. M. (1999) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19990105)62:1 · Cited by 322 · see citing works
Unearthing the roots of the terpenome
Christianson, D. W. (2008) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2007.12.008 · Cited by 318 · see citing works
Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation
Morant, M., Bak, S., Møller, B. L., et al. (2003) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(03)00024-7 · Cited by 296 · see citing works
Irmler, S., Schröder, G., St‐Pierre, B., Crouch, N. P., Hotze, M., Schmidt, J., Strack, D., Matern, U., & Schröder, J. (2000) · The Plant Journal · doi:10.1111/j.1365-313x.2000.00922.x · Cited by 273 · see citing works
Will Tribal Knowledge Survive the Millennium?
Cox, P. A. (2000) · Science · doi:10.1126/science.287.5450.44 · Cited by 272 · see citing works
Irmler, S., Schroder, G., St‐Pierre, B., Crouch, N. P., Hotze, M., Schmidt, J. G., Strack, D., Matern, U., & Schroder, J. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00922.x · Cited by 264 · see citing works
Yuan, L. Z., Rouvière, P. E., LaRossa, R. A., & Suh, W.-C. (2005) · Metabolic Engineering · doi:10.1016/j.ymben.2005.08.005 · Cited by 263 · see citing works
Newman, J. D., Marshall, J., Chang, M., Nowroozi, F., Paradise, E., Pitera, D., Newman, K. L., & Keasling, J. D. (2006) · Biotechnology and Bioengineering · doi:10.1002/bit.21017 · Cited by 257 · see citing works
Taxol: biosynthesis, molecular genetics, and biotechnological applications
Jennewein, S., & Croteau, R. (2001) · Applied Microbiology and Biotechnology · doi:10.1007/s002530100757 · Cited by 254 · see citing works
Tomato linalool synthase is induced in trichomes by jasmonic acid
van Schie, C. C. N., Haring, M. A., & Schuurink, R. C. (2007) · Plant Molecular Biology · doi:10.1007/s11103-007-9149-8 · Cited by 245 · see citing works
Lopez, A. B., Eck, J. M. V., Conlin, B. J., Paolillo, D. J., O'Neill, J., & Li, L. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/erm299 · Cited by 245 · see citing works
Schaller, H., Grausem, B., Benveniste, P., Chye, M. L., Tan, C. T., Song, Y. H., & Chua, N. H. (1995) · Plant Physiology · doi:10.1104/pp.109.3.761 · Cited by 230 · see citing works
Gustafson, K. R., Cardellina, J. H., McMahon, J. B., Gulakowski, R. J., Ishitoya, J., Szállási, Z., Lewin, N. E., Blumberg, P. M., & Weislow, O. S. (1992) · Journal of Medicinal Chemistry · doi:10.1021/jm00089a006 · Cited by 221 · see citing works
Oh, S. K., Kang, H., Shin, D. H., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.17132 · Cited by 218 · see citing works
Chemistry and biological activity of secondary metabolites in Euphorbia from Iran
Jassbi, A. R. (2006) · Phytochemistry · doi:10.1016/j.phytochem.2006.06.030 · Cited by 212 · see citing works
Steele, C. L., Gijzen, M., Qutob, D., et al. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1238 · Cited by 209 · see citing works
Hahn, F. M., Hurlburt, A. P., & Poulter, C. D. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.15.4499-4504.1999 · Cited by 206 · see citing works
Euphorbium: Modern research on its active principle, resiniferatoxin, revives an ancient medicine
Appendino, G., & SZALLASI, A. (1997) · Life Sciences · doi:10.1016/s0024-3205(96)00567-x · Cited by 199 · see citing works
Bak, S., Kahn, R. A., Nielsen, H. L., et al. (1998) · Plant Molecular Biology · doi:10.1023/a:1005915507497 · Cited by 196 · see citing works
Erbilgin, N., Krokene, P., Christiansen, E., et al. (2006) · Oecologia · doi:10.1007/s00442-006-0394-3 · Cited by 191 · see citing works
Bouvier, F., Suire, C., d’Harlingue, A., Backhaus, R. A., & Camara, B. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00875.x · Cited by 185 · see citing works
Application of Functional Genomics to Pathway Optimization for Increased Isoprenoid Production
Kizer, L., Pitera, D. J., Pfleger, B. F., & Keasling, J. D. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02750-07 · Cited by 178 · see citing works
Self-citationFollowing evolution's lead to a single residue switch for diterpene synthase product outcome
Xu, M., Wilderman, P. R., & Peters, R. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611454104 · Cited by 177 · see citing works
Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex
Chow, K. S., Wan, K., Isa, M. N. M., Bahari, A., Tan, S.-H., Harikrishna, K., & Yeang, H.-Y. (2007) · Journal of Experimental Botany · doi:10.1093/jxb/erm093 · Cited by 173 · see citing works
Muñoz‐Bertomeu, J., Arrillaga, I., Ros, R., & Segura, J. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.086355 · Cited by 171 · see citing works
Lupien, S. L., Karp, F., Wildung, M. R., & Croteau, R. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1298 · Cited by 170 · see citing works
Jennewein, S., Wildung, M. R., Chau, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403009101 · Cited by 168 · see citing works
Biosynthesis of terpenes: Studies on 1-hydroxy-2-methyl-2-( E )-butenyl 4-diphosphate reductase
Adam, P., Hecht, S., Eisenreich, W., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182412599 · Cited by 164 · see citing works
Characterization of recombinant plant cinnamate 4‐hydroxylase produced in yeast
Urban, P., Werck‐Reichhart, D., Teutsch, H., Durst, F., REGNIER, S., Kazmaier, M., & Pompon, D. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.tb18931.x · Cited by 163 · see citing works
Evidence of a Role for LytB in the Nonmevalonate Pathway of Isoprenoid Biosynthesis
Cunningham, F. X., Lafond, T. P., & Gantt, E. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.20.5841-5848.2000 · Cited by 163 · see citing works
Shibuya, M., Hoshino, M., Katsube, Y., et al. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2006.05120.x · Cited by 161 · see citing works
Reflections on the ‘discovery’ of the antimalarial qinghao
Hsü, E. (2006) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2006.02673.x · Cited by 155 · see citing works
Bezemer, Т. M., Wagenaar, R., van Dam, N. M., et al. (2004) · Journal of Chemical Ecology · doi:10.1023/b:joec.0000013182.50662.2a · Cited by 150 · see citing works
Gardner, R. G., & Hampton, R. Y. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.44.31671 · Cited by 149 · see citing works
Paradise, E. M., Kirby, J., Chan, R., & Keasling, J. D. (2008) · Biotechnology and Bioengineering · doi:10.1002/bit.21766 · Cited by 148 · see citing works
Self-citationA P450 BM-3 mutant hydroxylates alkanes, cycloalkanes, arenes and heteroarenes
Appel, D., Lutz‐Wahl, S., Fischer, P., et al. (2001) · Journal of Biotechnology · doi:10.1016/s0168-1656(01)00249-8 · Cited by 142 · see citing works
Multi-dimensional gene target search for improving lycopene biosynthesis in Escherichia coli
Jin, Y., & Stephanopoulos, G. N. (2007) · Metabolic Engineering · doi:10.1016/j.ymben.2007.03.003 · Cited by 139 · see citing works
The Ethnobotanical Approach to Drug Discovery: Strengths and Limitations
Cox, P. A. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514634.ch3 · Cited by 132 · see citing works
Ohnuma, S., Narita, K., Nakazawa, T., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.48.30748 · Cited by 132 · see citing works
Ríos‐Estepa, R., Turner, G. W., Lee, J. M., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712314105 · Cited by 132 · see citing works
Hale, V., Keasling, J. D., Renninger, N. S., & Diagana, T. T. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.77.198 · Cited by 131 · see citing works
Self-citationNishizaki, T., Tsuge, K., Itaya, M., et al. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.02268-06 · Cited by 129 · see citing works
Molecular Recognition in (+)-α-Pinene Oxidation by Cytochrome P450cam
Bell, S. G., Chen, X., Sowden, R. J., et al. (2002) · Journal of the American Chemical Society · doi:10.1021/ja028460a · Cited by 120 · see citing works
Microbial Isoprenoid Production: An Example of Green Chemistry through Metabolic Engineering
Maury, J., Asadollahi, M. A., Møller, K., Clark, A., & Nielsen, J. (2005) · Advances in biochemical engineering, biotechnology · doi:10.1007/b136410 · Cited by 119 · see citing works
Hotze, M., Schröder, G., & Schröder, J. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)01141-z · Cited by 119 · see citing works
Metabolic engineering of carotenoid accumulation by creating a metabolic sink
Li, L., & Eck, J. M. V. (2007) · Transgenic Research · doi:10.1007/s11248-007-9111-1 · Cited by 117 · see citing works
Page, J. E., Hause, G., Raschke, M., Gao, W., Schmidt, J., Zenk, M. H., & Kutchan, T. M. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.038133 · Cited by 117 · see citing works
Why Is Golden Rice Golden (Yellow) Instead of Red?
Schaub, P., Al‐Babili, S., Drake, R., & Beyer, P. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.057927 · Cited by 116 · see citing works
Increased Terpenoid Accumulation in Cotton (Gossypium hirsutum) Foliage is a General Wound Response
Opitz, S., Kunert, G., & Gershenzon, J. (2008) · Journal of Chemical Ecology · doi:10.1007/s10886-008-9453-z · Cited by 111 · see citing works
Functional Evolution and Structural Conservation in Chimeric Cytochromes P450
Otey, C. R., Silberg, J. J., Voigt, C. A., Endelman, J. B., Bandara, G., & Arnold, F. H. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.02.018 · Cited by 109 · see citing works
Gillam, E. M. J., Guo, Z., Martin, M. V., Jenkins, C. M., & Guengerich, F. P. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1329 · Cited by 104 · see citing works
Engineering Cotton (+)-δ-Cadinene Synthase to an Altered Function: Germacrene D-4-ol Synthase
Yoshikuni, Y., Martin, V. J. J., Ferrin, T. E., et al. (2006) · Chemistry & Biology · doi:10.1016/j.chembiol.2005.10.016 · Cited by 101 · see citing works
Increasing Expression of P450 and P450-Reductase Proteins from Monocots in Heterologous Systems
Batard, Y., Hehn, A., Nedelkina, S., Schalk, M., Pallett, K. E., Schaller, H., & Werck‐Reichhart, D. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.1867 · Cited by 94 · see citing works
Production of Paclitaxel and the Related Taxanes by Cell Suspension Cultures of Taxus Species
Tabata, H. (2006) · Current Drug Targets · doi:10.2174/138945006776359368 · Cited by 93 · see citing works
Identification of genes affecting lycopene accumulation in Escherichia coli using a shot‐gun method
Kang, M., Lee, Y. M., Yoon, S. H., Kim, J. H., Ock, S. W., Jung, K. H., Shin, Y. C., Keasling, J. D., & Kim, S. W. (2005) · Biotechnology and Bioengineering · doi:10.1002/bit.20539 · Cited by 93 · see citing works
Self-citationMicrobial sensors for small molecules: Development of a mevalonate biosensor
Pfleger, B. F., Pitera, D. J., Newman, J. D., et al. (2006) · Metabolic Engineering · doi:10.1016/j.ymben.2006.08.002 · Cited by 88 · see citing works
Mutagenesis approaches to deduce structure–function relationships in terpene synthases
Segura, M. J. R., Jackson, B. E., & Matsuda, S. P. T. (2003) · Natural Product Reports · doi:10.1039/b008338k · Cited by 86 · see citing works
McAuslane, H. J., Alborn, H. T., & Toth, J. P. (1997) · Journal of Chemical Ecology · doi:10.1023/a:1022575313325 · Cited by 81 · see citing works
Characterization of lycopene-overproducing E. coli strains in high cell density fermentations
Alper, H. S., Miyaoku, K., & Stephanopoulos, G. N. (2006) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-006-0357-y · Cited by 78 · see citing works
Gong, Y., Liao, Z., Guo, B., et al. (2006) · Planta Medica · doi:10.1055/s-2005-916234 · Cited by 76 · see citing works
Production of lipid compounds in the yeast Saccharomyces cerevisiae
Veen, M., & Lang, C. (2004) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-003-1456-7 · Cited by 65 · see citing works
Hannemann, F., Virus, C., & Bernhardt, R. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.01.009 · Cited by 62 · see citing works
How to make taxol from scratch
Horwitz, S. B. (1994) · Nature · doi:10.1038/367593a0 · Cited by 61 · see citing works
Priya, P., Venkatachalam, P., & Thulaseedharan, A. (2007) · Plant Cell Reports · doi:10.1007/s00299-007-0402-z · Cited by 59 · see citing works
Improved cloning and expression of cytochrome P450s and cytochrome P450 reductase in yeast
Hamann, T., & Møller, B. L. (2007) · Protein Expression and Purification · doi:10.1016/j.pep.2007.06.007 · Cited by 54 · see citing works
Khemvong, S., & Suvachittanont, W. (2005) · Plant Science · doi:10.1016/j.plantsci.2005.05.001 · Cited by 48 · see citing works
Design of a Novel P450: A Functional Bacterial−Human Cytochrome P450 Chimera
Shimoji, M., Yin, H., Higgins, L., & Jones, J. P. (1998) · Biochemistry · doi:10.1021/bi972775z · Cited by 27 · see citing works
A Novel Saponin Hydrolase from Neocosmospora vasinfecta var. vasinfecta
Watanabe, M., Sumida, N., Yanai, K., et al. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.2.865-872.2004 · Cited by 19 · see citing works
Vroom, J. A., & Wang, C. L. (2008) · BioTechniques · doi:10.2144/000112808 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biofuels from algae: Challenges and potential
Hannon, M., Gimpel, J., Tran, M., Rasala, B., & Mayfield, S. (2010) · Biofuels · doi:10.4155/bfs.10.44 · Cited by 813 · see citing works
Isoprenoid drugs, biofuels, and Chemicals–Artemisinin, farnesene, and beyond
George, K. W., Alonso-Gutierrez, J., Keasling, J. D., & Lee, T. S. (2015) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2014_288 · Cited by 185 · see citing works
Self-citationBeyond malaria: The inhibition of viruses by artemisinin-type compounds
Efferth, T. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.01.001 · Cited by 157 · see citing works
Lauersen, K. J., Wichmann, J., Baier, T., Kampranis, S. C., Pateraki, I., Møller, B. L., & Kruse, O. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.07.005 · Cited by 124 · see citing works
Cataldo, V. F., López, J., Cárcamo, M., & Agosin, E. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7583-8 · Cited by 77 · see citing works
Production of (−)-α-Bisabolol in Metabolically Engineered Saccharomyces Cerevisiae
Kim, T. Y., Park, H., Kim, S.-K., Kim, S.-J., & Park, Y.-C. (2021) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2021.08.008 · Cited by 23 · see citing works
Suberu, J., Gromski, P. S., Nordon, A., & Lapkin, A. (2016) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2015.10.003 · Cited by 19 · see citing works
- Authors
- Kirby, J., & Keasling, J. D.
- Affiliations
- University of California, Berkeley (US)
- Lawrence Berkeley National Laboratory (US)
- Venue
- Annual Review of Plant Biology
- Publisher
- Annual Reviews
- Published
- 2009-06-01
- Volume
- 60
- Issue
- 1
- Pages
- 335-355
- ISSN
- 1543-5008 (ISSN-L)
- 1545-2123
- OpenAlex
- W2143814332
- Cited by
- 478
- References
- 105
- Citations by year
- 2026: 22 · 2025: 18 · 2024: 23 · 2023: 21 · 2022: 33 · 2021: 25 · 2020: 34 · 2019: 23 · 2018: 32 · 2017: 34 · 2016: 26 · 2015: 33 · 2014: 34 · 2013: 36 · 2012: 31
- FWCI
- 2.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Plant Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
- Keywords
- terpenoids, isoprenoid biosynthesis, terpene synthase, cytochrome P450 monooxygenase, microbial engineering, pathway engineering, plant secondary metabolism, gene discovery, heterologous expression
- MeSH terms
- Cytochrome P-450 Enzyme System, Mutation, Plants, Terpenes, Gene Expression, Genes, Plant
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review