Branch pathway blocking in artemisia annua is a useful method for obtaining high yield artemisinin

Plant and Cell Physiology

Volumn 57, Issue 3, 2016, Pages 588-602

  Lv, Zongyou ^a   Zhang, Fangyuan ^a   Pan, Qifang ^a   Fu, Xueqing ^a   Jiang, Weimin ^a   Shen, Qian ^a   Yan, Tingxiang ^a   Shi, Pu ^a   Lu, Xu ^a   Sun, Xiaofen ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Antisense; Artemisia annua L; Artemisinin biosynthesis; Germacrene A synthase (GAS); Squalene synthase (SQS); Caryophyllene synthase (CPS); farnesene synthase (BFS)

Indexed keywords

ARTEMISIN; ARTEMISININ DERIVATIVE; BETA-FARNESENE; BETA-FARNESENE SYNTHASE; CARYOPHYLLENE; INORGANIC PYROPHOSPHATASE; LACTONE; PLANT PROTEIN; SESQUITERPENE; SQUALENE; SQUALENE SYNTHASE; TERPENE;

ANTAGONISTS AND INHIBITORS; ARTEMISIA ANNUA; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT GENE; TRANSGENIC PLANT;

ARTEMISIA ANNUA; ARTEMISININS; BIOSYNTHETIC PATHWAYS; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LACTONES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PYROPHOSPHATASES; SESQUITERPENES; SQUALENE; TERPENES;

EID: 84963972541     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcw014     Document Type: Article

References (53)

1. Allen G.C, Flores-Vergara M.A, Krasynanski S, Kumar S, and Thompson W.F. (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat. Protoc. 1: 2320-2325.
2. Anthony J.R, Anthony L.C, Nowroozi F, Kwon G, Newman J.D, and Keasling J.D. (2009). Optimization of the mevalonate-based isoprenoid biosynthetic pathway in Escherichia coli for production of the antimalarial drug precursor amorpha-4, 11-diene. Metab. Eng. 11: 13-19.
3. Arsenault P.R, Vail D, Wobbe K.K, Erickson K, and Weathers P.J. (2010). Reproductive development modulates gene expression and metabolite levels with possible feedback inhibition of artemisinin in Artemisia annua. Plant Physiol. 154: 958-968.
4. Beale M.H, Birkett M.A, Bruce T.J, Chamberlain K, Field L.M, Huttly A.K, et al. (2006). Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc. Natl. Acad. Sci. USA. 103: 10509-10513.
5. Bertea C.M, Voster A, Verstappen F.W.A, Maffei M, Beekwilder J, and Bouwmeester H.J. (2006). Isoprenoid biosynthesis in Artemisia annua: cloning and heterologous expression of a germacrene A synthase from a glandular trichome cDNA library. Arch. Biochem. Biophys. 448: 3-12.
6. Bouwmeester H.J, Wallaart T.E, Janssen M.H.A, van Loo B, Jansen B.J.M, Posthumus M.A, et al. (1999). Amorpha-4, 11-diene synthase catalyses the first probable step in artemisinin biosynthesis. Phytochemistry. 52: 843-854.
7. Bowers W.S, Nishino C, Montgomery M.E, Nault L.R, and Nielson M.W. (1977). Sesquiterpene progenitor, germacrene A: an alarm pheromone in aphids. Science. 196: 680-681.
8. Brown G.D. (2010). The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules. 15: 7603-7698.
9. Cai Y, Jia J.W, Crock J, Lin Z.X, Chen X.Y, and Croteau R. (2002) A cDNA clone for [beta]-caryophyllene synthase from Artemisia annua. Phytochemistry. 61: 523-529.
10. Caretto S, Quarta A, Durante M, Nisi R, De Paolis A, Blando F, et al. (2011). Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol. 13: 51-58.
11. Chen J.L, Fang H.M, Ji Y.P, Pu G.B, Guo Y.W, Huang L.L, et al. (2011). Artemisinin biosynthesis enhancement in transgenic Artemisia annua plants by downregulation of the b-caryophyllene synthase gene. Planta Med. 77: 1759-1765.
12. Covello P.S. (2008). Making artemisinin. Phytochemistry. 69: 2881-2885.
13. Devarenne T.P, Ghosh A, and Chappell J. (2002). Regulation of squalene synthase, a key enzyme of sterol biosynthesis, in tobacco. Plant Physiol. 129: 1095-1106.
14. Francis F, Vandermoten S, Verheggen F, Lognay G, and Haubruge E. (2005). Is the (E)-b-farnesene only volatile terpenoid in aphids?. J. Appl. Entomol. 129: 6-11.
15. Graham I.A, Besser K, Blumer S, Branigan C.A, Czechowski T, Elias L, et al. (2010). The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science. 327: 328-331.
16. Gunde-Cimerman N, Friedrich J, Cimerman A, and Benički N. (1993). Screening fungi for the production of an inhibitor of HMG CoA reductase: production of mevinolin by the fungi of the genus Pleurotus. FEMS Microbiol. Lett. 111: 203-206.
17. Jiang W, Lu X, Qiu B, Zhang F, Shen Q, Lv Z, et al. (2014). Molecular cloning and characterization of a trichome-specific promoter of artemisinic aldehyde 11 (13) reductase (DBR2) in Artemisia annua. Plant. Mol. Biol. Rep. 32: 82-91.
18. Kim S, Chang Y, and Kim S. (2008). Tissue specificity and developmental pattern of amorpha-4, 11-diene synthase (ADS) proved by ADS promoter-driven GUS expression in the heterologous plant. Arabidopsis thaliana, Planta Med. 74: 188-193.
19. Köllner T.G, Held M, Lenk C, Hiltpold I, Turlings T.C, Gershenzon J, et al. (2008) A maize (E)-b-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell. 20: 482-494.
20. Komori A, Suzuki M, Seki H, Nishizawa T, Meyer J.J.M, Shimizu H, et al. (2013). Comparative functional analysis of CYP71AV1 natural variants reveals an important residue for the successive oxidation of amorpha-4, 11-diene. FEBS Lett. 587: 278-284.
21. Kuzuyama T, Shimizu T, Takahashi S, and Seto H. (1998). Fosmidomycin, a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett. 39: 7913-7916.
22. Lommen W.J, Elzinga S, Verstappen F.W, and Bouwmeester H.J. (2007). Artemisinin and sesquiterpene precursors in dead and green leaves of Artemisia annua L. crops. Planta Med. 73: 1133-1139.
23. Lu X, Zhang L, Zhang F, Jiang W, Shen Q, Zhang L, et al. (2013). AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytol. 198: 1191-1202.
24. Ma C, Wang H, Lu X, Wang H, Xu G, and Liu B. (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.
25. Manavalan L.P, Chen X, Clarke J, Salmeron J, and Nguyen H.T. (2012). RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J. Exp. Bot. 63: 163-175.
26. Mercke P, Bengtsson M, Bouwmeester H.J, Posthumus M.A, and Brodelius P.E. (2000). Molecular cloning, expression, and characterization of amorpha-4, 11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L. Arch. Biochem. Biophys. 381: 173-180.
27. Mercke P, Crock J, Croteau R, and Brodelius P.E. (1999). Cloning, expression, and characterization of epi-cedrol synthase, a sesquiterpene cyclase from Artemisia annua L. Arch. Biochem. Biophys. 369: 213-222.
28. Murashige T, and Skoog F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 3: 473-497.
29. Olofsson L, Engström A, Lundgren A, and Brodelius P.E. (2011). Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol. 11: 45.
30. Olsson M.E, Olofsson L.M, Lindahl A.L, Lundgren A, Brodelius M, and Brodelius P.E. (2009). Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry. 70: 1123-1128.
31. Picaud S, Brodelius M, and Brodelius P.E. (2005). Expression, purification and characterization of recombinant (E)-[beta]-farnesene synthase from Artemisia annua. Phytochemistry. 66: 961-967.
32. Ro D.K, Paradise E.M, Ouellet M, Fisher K.J, Newman K.L, Ndungu J.M, et al. (2006). Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature. 440: 940-943.
33. Rydén A, Ruyter-Spira C, Quax W.J, Osada H, Muranaka T, Kayser O, et al. (2010). The molecular cloning of dihydroartemisinic aldehyde reductase and its implication in artemisinin biosynthesis in Artemisia annua. Planta Med. 76: 1778.
34. Schramek N, Wang H, Römisch-Margl W, Keil B, Radykewicz T, Winzenhörlein B, et al. (2010). Artemisinin biosynthesis in growing plants of Artemisia annua A 13CO2 study. Phytochemistry. 71: 179-187.
35. Shen Q, Chen Y.F, Wang T, Wu S.Y, Lu X, Zhang L, et al. (2012). Overexpression of the cytochrome P450 monooxygenase (CYP71AV1) and cytochrome P450 reductase (CPR) genes increased artemisinin content in Artemisia annua (Asteraceae). Genet. Mol. Res. 11: 3298-3309.
36. Tang K, Shen Q, Yan T, and Fu X. (2014). Transgenic approach to increase artemisinin content in Artemisia annua L. Plant Cell Rep. 33: 605-615.
37. Tellez M.R, Canel C, Rimando A.M, and Duke S.O. (1999). Differential accumulation of isoprenoids in glanded and glandless Artemisia annua L. Phytochemistry. 52: 1035-1040.
38. Teoh K.H, Polichuk D.R, Reed D.W, Nowak G, and Covello P.S. (2006). Artemisia annua L.(Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett. 580: 1411-1416.
39. Teoh K.H.T.K, Polichuk D.R.P.D, Reed D.W.R.D, and Covello P.S.C.P. (2009). Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany. 87: 635-642.
40. Ting H.M, Wang B, Rydén A.M, Woittiez L, Herpen T, Verstappen F.W, et al. (2013). The metabolite chemotype of Nicotiana benthamiana transiently expressing artemisinin biosynthetic pathway genes is a function of CYP71AV1 type and relative gene dosage. New Phytol. 199: 352-366.
41. Towler M.J, and Weathers P.J. (2007). Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep. 26: 2129-2136.
42. Tran K.Q, Tin A.S, and Firestone G.L. (2014). Artemisinin triggers a G1 cell cycle arrest of human Ishikawa endometrial cancer cells and inhibits cyclin-dependent kinase-4 promoter activity and expression by disrupting nuclear factor-kB transcriptional signaling. Anti-Cancer Drug. 25: 270-281.
43. Wang H, Han J, Kanagarajan S, Lundgren A, and Brodelius P.E. (2013). Studies on the expression of sesquiterpene synthases using promoter-b-glucuronidase fusions in transgenic Artemisia annua L. PLoS One. 8: e80643.
44. Wang H, Han J, Kanagarajan S, Lundgren A, and Brodelius P.E. (2013). Trichome-specific expression of the amorpha-4, 11-diene 12-hydroxylase (CYP71AV1) gene, encoding a key enzyme of artemisinin biosynthesis in Artemisia annua, as reported by a promoter-GUS fusion. Plant Mol. Biol. 81: 119-138.
45. Wang H, Ma C, Ma L, Du Z, Wang H, and Ye H, et al. (2009). Secondary metabolic profiling and artemisinin biosynthesis of two genotypes of Artemisia annua. Planta Med. 75: 1625-1633.
46. Wang H, Olofsson L, Lundgren A, and Brodelius P.E. (2011). Trichomespecific expression of amorpha-4, 11-diene synthase, a key knzyme of artemisinin biosynthesis in Artemisia annua L, as reported by a promoter-GUS fusion. Amer. J. Plant Sci. 2: 619-628.
47. Wang W, Vinocur B, Shoseyov O, and Altman A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9: 244-252.
48. Westfall P.J, Pitera D.J, Lenihan J.R, Eng D, Woolard F.X, Regentin R, 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: E111-E118.
49. Zhang F, Fu X, Lv Z, Lu X, Shen Q, Zhang L, et al. (2015) A basic leucine zipper transcription factor, AabZIP1, connects abscisic acid signaling with artemisinin biosynthesis in Artemisia annua. Mol. Plant. 8: 163-175.
50. Zhang L, Jing F, Li F, Li M, Wang Y, Wang G, et al. (2009). Development of transgenic Artemisia annua (Chinese wormwood) plants with an enhanced content of artemisinin, an effective antimalarial drug, by hairpin-RNA-mediated gene silencing. Biotechnol. Appl. Biochem. 52: 199-207.
51. Zhang L, Lu X, Shen Q, Chen Y, Wang T, Zhang F, et al. (2012). Identification of putative Artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and in response to methyl jasmonate and abscisic acid treatments. Plant Mol. Biol. Rep. 30: 838-847.
52. Zhang Y, Teoh K.H, Reed D.W, Maes L, Goossens A, Olson D.J.H, et al. (2008). The molecular cloning of artemisinic aldehyde 11 (13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J. Biol. Chem. 283: 21501.
53. Zhu M, Zhang F, Lv Z, Shen Q, Zhang L, Lu X, et al. (2013). Characterization of the promoter of Artemisia annua amorpha-4, 11-diene synthase (ADS) gene using homologous and heterologous expression as well as deletion analysis. Plant Mol. Biol. Rep. 32: 406-418.