(+)-Valencene production in Nicotiana benthamiana is increased by down-regulation of competing pathways

Biotechnology Journal

Volumn 10, Issue 1, 2015, Pages 180-189

  Cankar, Katarina ^a   Jongedijk, Esmer ^a   Klompmaker, Martin ^a   Majdic, Timotej ^a   Mumm, Roland ^a   Bouwmeester, Harro ^a   Bosch, Dirk ^a   Beekwilder, Jules ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

(+) Valencene; 5 Epi aristolochene synthase; Metabolic engineering; RNAi; Squalene synthase

Indexed keywords

BIOCHEMISTRY; LAKES; METABOLIC ENGINEERING; METABOLISM; OLEFINS;

BENTHAMIANA PLANTS; BREAKDOWN PRODUCTS; FARNESYL DIPHOSPHATE; NICOTIANA BENTHAMIANA; RNAI; SYNTHASES; VALENCENE; VALUABLE CHEMICALS;

PLANTS (BOTANY);

5 EPI ARISTOLOCHENE SYNTHASE; ARISTOLOCHENE; FARNESOL; GERANYLTRANSFERASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; SQUALENE SYNTHASE; UNCLASSIFIED DRUG; VALENCENE; FARNESYL DIPHOSPHATE; ISOPRENOID PHOSPHATE; SESQUITERPENE; TRANSFERASE; VEGETABLE PROTEIN;

ANALYTIC METHOD; ARTICLE; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; BIOTECHNOLOGICAL PRODUCTION; CYTOSOL; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; METABOLIC ENGINEERING; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT GENOME; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; GENETICS; METABOLISM; PROCEDURES; RNA INTERFERENCE; TOBACCO; TRANSGENIC PLANT;

NICOTIANA BENTHAMIANA;

ALKYL AND ARYL TRANSFERASES; DOWN-REGULATION; GERANYLTRANSTRANSFERASE; HYDROXYMETHYLGLUTARYL COA REDUCTASES; METABOLIC ENGINEERING; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLYISOPRENYL PHOSPHATES; RNA INTERFERENCE; SESQUITERPENES; TOBACCO;

EID: 84921451541     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400288     Document Type: Article

References (39)

1. Gershenzon, J., Dudareva, N., The function of terpene natural products in the natural world. Nat. Chem. Biol. 2007, 3, 408-414.
2. Gershenzon, J., Kreis, W., Biochemistry of terpenoids: Monoterpenes, sesquiterpenes, diterpenes, sterols, cardiac glycosides and steroid saponins. in: Wink, M. (Ed.), Biochemistry of Plant Secondary Metabolism, Sheffield Academic Press, Sheffield 1999, pp. 222-299.
3. Kappers, I. F., Aharoni, A., van Herpen, T. W. J. M., Luckerhoff, L. L. P. et al., Genetic engineering of terpenoid metabolism attracts, bodyguards to Arabidopsis. Science 2005, 309, 2070-2072.
4. Houshyani, B., Assareh, M., Busquets, A., Ferrer, A. et al., Three-step pathway engineering results in more incidence rate and higher emission of nerolidol and improved attraction of Diadegma semiclausum. Metab. Eng. 2013, 15, 88-97.
5. Schnee, C., Kollner, T. G., Held, M., Turlings, T. C. J. et al., The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. USA 2006, 103, 1129-1134.
6. van Herpen, T. W. J. M., Cankar, K., Nogueira, M., Bosch, D. et al., Nicotiana benthamiana as a production platform for artemisinin precursors. PLos ONE 2010, 5, e14222.
7. Zhang, Y. S., Nowak, G., Reed, D. W., Covello, P. S., The production of artemisinin precursors in tobacco. Plant Biotechnol. J. 2011, 9, 445-454.
8. Ting, H. M., Wang, B., Ryden, A. M., Woittiez, L. et al., The metabolite chemotype of Nicotiana benthamiana transiently expressing artemisinin biosynthetic pathway genes is a function of CYP71AV1 type and relative gene dosage. New Phytol. 2013, 199, 352-366.
9. Wu, S. Q., Schalk, M., Clark, A., Miles, R. B. et al., Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotechnol. 2006, 24, 1441-1447.
10. Wu, S., Jiang, Z., Kempinski, C., Eric Nybo, S. et al., Engineering triterpene metabolism in tobacco. Planta 2012, 236, 867-877.
11. Lucker, J., Schwab, W., van Hautum, B., Blaas, J. et al., Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol. 2004, 134, 510-519.
12. Giritch, A., Marillonnet, S., Engler, C., van Eldik, G. et al., Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc. Natl. Acad. Sci. USA 2006, 103, 14701-14706.
13. Mikkelsen, M. D., Olsen, C. E., Halkier, B. A., Production of the cancer-preventive glucoraphanin in tobacco. Mol. Plant 2010, 3, 751-759.
14. Naim, F., Nakasugi, K., Crowhurst, R. N., Hilario, E. et al., Advanced engineering of lipid metabolism in Nicotiana benthamiana using a draft genome and the V2 viral silencing-suppressor protein. PLoS ONE 2012, 7, e52717.
15. Liu, Q., Majdi, M., Cankar, K., Goedbloed, M. et al., Reconstitution of the costunolide biosynthetic pathway in yeast and Nicotiana benthamiana. PLoS ONE 2011, 6, e23255.
16. Chappell, J., The genetics and molecular genetics of terpene and sterol origami. Curr. Opin. Plant Biol. 2002, 5, 151-157.
17. Wallaart, T. E., Bouwmeester, H. J., Hille, J., Poppinga, L., Maijers, N. C. A., Amorpha-4, 11-diene synthase: Cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 2001, 212, 460-465.
18. Scalcinati, G., Partow, S., Siewers, V., Schalk, M. et al., Combined metabolic engineering of precursor and co-factor supply to increase alpha-santalene production by Saccharomyces cerevisiae. Microb. Cell Fact. 2012, 11, 117.
19. Ro, D. K., Paradise, E. M., Ouellet, M., Fisher, K. J. et al., Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440, 940-943.
20. Bombarely, A., Rosli, H. G., Vrebalov, J., Moffett, P. et al., A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol. Plant Microbe Interact. 2012, 25, 1523-1530.
21. Beekwilder, J., van Houwelingen, A., Cankar, K., van Dijk, A. D. J. et al., Valencene synthase from the heartwood of Nootka cypress (Callitropsis nootkatensis) for biotechnological production of valencene. Plant Biotechnol. J. 2014, 12, 174-182.
22. Facchini, P. J., Chappell, J., Gene family for an elicitor-induced sesquiterpene cyclase in tobacco. Proc. Natl. Acad. Sci. USA 1992, 89, 11088-11092.
23. Devarenne, T. P., Shin, D. H., Back, K., Yin, S. H., Chappell, J., Molecular characterization of tobacco squalene synthase and regulation in response to fungal elicitor. Arch. Biochem. Biophys. 1998, 349, 205-215.
24. Karimi, M., Inze, D., Depicker, A., GATEWAY((TM)) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002, 7, 193-195.
25. Outchkourov, N. S., Peters, J., de Jong, J., Rademakers, W., Jongsma, M. A., The promoter-terminator of chrysanthemum rbcS1 directs very high expression levels in plants. Planta 2003, 216, 1003-1012.
26. Vanengelen, F. A., Molthoff, J. W., Conner, A. J., Nap, J. P. et al., Pbinplus - an improved plant transformation vector based on Pbin19. Transgenic Res. 1995, 4, 288-290.
27. Snoeren, T. A. L., Kappers, I. F., Broekgaarden, C., Mumm, R. et al., Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J. Exp. Bot. 2010, 61, 3041-3056.
28. Lu, Y. Q., Xie, L. L., Chen, J. N., A novel procedure for absolute real-time quantification of gene expression patterns. Plant Methods 2012, 8, 9.
29. Aharoni, A., Giri, A. P., Deuerlein, S., Griepink, F. et al., Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 2003, 15, 2866-2884.
30. Meigs, T. E., Simoni, R. D., Farnesol as a regulator of HMG-CoA reductase degradation: Characterization and role of farnesyl pyrophosphatase. Arch. Biochem. Biophys. 1997, 345, 1-9.
31. Wentzinger, L. F., Bach, T. J., Hartmann, M. A., Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol. 2002, 130, 334-346.
32. Hemmerlin, A., Bach, T. J., Farnesol-induced cell death and stimulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase activity in tobacco cv Bright Yellow-2 cells. Plant Physiol. 2000, 123, 1257-1268.
33. Rising, K. A., Starks, C. M., Noel, J. P., Chappell, J., Demonstration of germacrene A as an intermediate in 5-epi-aristolochene synthase catalysis. J. Am. Chem. Soc. 2000, 122, 1861-1866.
34. Zhang, D., Jennings, S. M., Robinson, G. W., Poulter, C. D., Yeast squalene synthase - expression, purification, and characterization of soluble recombinant enzyme. Arch. Biochem. Biophys. 1993, 305, 622-622.
35. Voinnet, O., Rivas, S., Mestre, P., Baulcombe, D., An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003, 33, 949-956.
36. Zrachya, A., Glick, E., Levy, Y., Arazi, T. et al., Suppressor of RNA silencing encoded by tomato yellow leaf curl virus-Israel. Virology 2007, 358, 159-165.
37. Peralta-Yahya, P. P., Ouellet, M., Chan, R., Mukhopadhyay, A. et al., Identification and microbial production of a terpene-based advanced biofuel. Nat. Commun. 2011, 2, 483.
38. Paddon, C. J., Westfall, P. J., Pitera, D. J., Benjamin, K. et al., High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496, 528-532.
39. Mahroug, S., Burlat, V., St-Pierre, B., Cellular and sub-cellular organisation of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Phytochem. Rev. 2007, 6, 363-381.