Overexpression of AaWRKY1 Leads to an Enhanced Content of Artemisinin in Artemisia annua

BioMed Research International

Volumn 2016, Issue , 2016, Pages

  Jiang, Weimin ^a   Fu, Xueqing ^a   Pan, Qifang ^a   Tang, Yueli ^a   Shen, Qian ^a   Lv, Zongyou ^a   Yan, Tingxiang ^a   Shi, Pu ^a   Li, Ling ^a   Zhang, Lida ^a   Wang, Guofeng ^a   Sun, Xiaofen ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AAWRKY1 PROTEIN; AMORPHA 4,11 DIENE SYNTHASE; ARTEMISININ; CYTOCHROME P450; LUCIFERASE; SYNTHETASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARTEMISININ DERIVATIVE; DNA BINDING PROTEIN; PLANT PROTEIN;

ARTEMISIA ANNUA; ARTICLE; CONTROLLED STUDY; DRUG SYNTHESIS; EXPRESSION VECTOR; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; LUCIFERASE ASSAY; NONHUMAN; PROMOTER REGION; TOBACCO; TRANSGENIC PLANT; GENETICS; METABOLISM; MOLECULAR CLONING;

ARTEMISIA ANNUA; ARTEMISININS; CLONING, MOLECULAR; DNA-BINDING PROTEINS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84960981829     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2016/7314971     Document Type: Article

References (63)

1. E. Hsu, "The history of qing hao in theChinesemateria medica," Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 100, no. 6, pp. 505-508, 2006.
2. L. H. Miller and X. Su, "Artemisinin: discovery fromtheChinese herbal garden," Cell, vol. 146, no. 6, pp. 855-858, 2011.
3. A. Bhattarai,A. S. Ali, S. P. Kachur et al., "Impact of artemisininbased combination therapy and insecticide-treated nets on malaria burden in Zanzibar," PLoS Medicine, vol. 4, no. 11, pp. 1784-1790, 2007.
4. N. P. Singh and H. C. Lai, "Artemisinin induces apoptosis in human cancer cells," Anticancer Research, vol. 24, no. 4, pp. 2277-2280, 2004.
5. M. R. Romero, T. Efferth, M. A. Serrano et al., "Effect of artemisinin/artesunate as inhibitors of hepatitis B virus production in an 'in vitro' replicative system," Antiviral Research, vol. 68, no. 2, pp. 75-83, 2005.
6. P. S. Covello, K. H. Teoh, D. R. Polichuk, D. W. Reed, and G. Nowak, "Functional genomics and the biosynthesis of artemisinin," Phytochemistry, vol. 68,no. 14,pp. 1864-1871, 2007.
7. P. R. Arsenault, D. Vail, K. K. Wobbe, K. Erickson, and P. J. Weathers, "Reproductive development modulates gene expression and metabolite levels with possible feedback inhibition of artemisinin in Artemisia annua," Plant Physiology, vol. 154, no. 2, pp. 958-968, 2010.
8. M. J. Towler and P. J. Weathers, "Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways," Plant Cell Reports, vol. 26, no. 12, pp. 2129-2136, 2007.
9. J. Chappell,F. Wolf, J. Proulx,R. Cuellar, andC. Saunders, "Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plants" Plant Physiology, vol. 109, no. 4, pp. 1337-1343, 1995.
10. H. Schaller, B. Grausem, P. Benveniste et al., "Expression of the Hevea brasiliensis (H. B. K. ) Müll. Arg. 3-hydroxy-3-methylglutaryl-coenzyme A reductase 1 in tobacco results in sterol overproduction," Plant Physiology, vol. 109, no. 3, pp. 761-770, 1995.
11. H. J. Bouwmeester, T. E. Wallaart, M. H. A. Janssen et al., "Amorpha-4,11-diene synthase catalyses the first probable step in artemisinin biosynthesis," Phytochemistry, vol. 52, no. 5, pp. 843-854, 1999.
12. T. E. Wallaart, H. J. Bouwmeester, J. Hille, L. Poppinga, and N. C. A. Maijers, "Amorpha-4,11-diene synthase: cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin," Planta, vol. 212, no. 3, pp. 460-465, 2001.
13. K. H. Teoh, D. R. Polichuk, D. W. Reed, G. Nowak, and P. S. Covello, "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 Letters, vol. 580, no. 5, pp. 1411-1416, 2006.
14. Y. Zhang, K. H. Teoh, D. W. Reed et al., "The molecular cloning of artemisinic aldehyde 11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua," The Journal of Biological Chemistry, vol. 283, no. 31, pp. 21501-21508, 2008.
15. K. H. Teoh, D. R. Polichuk, D. W. Reed, and P. S. Covello, "Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua," Botany, vol. 87, no. 6, pp. 635-642, 2009.
16. L.-K. Sy and G. D. Brown, "The mechanism of the spontaneous autoxidation of dihydroartemisinic acid," Tetrahedron, vol. 58, no. 5, pp. 897-908, 2002.
17. S.-H. Kim, Y.-J. Chang, and S.-U. Kim, "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 Medica, vol. 74, no. 2, pp. 188-193, 2008.
18. H. Wang, J. Han, S. Kanagarajan, A. Lundgren, and P. E. Brodelius, "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 Molecular Biology, vol. 81, no. 1-2, pp. 119-138, 2013.
19. H. Wang, L. Olofsson, A. Lundgren, and P. E. Brodelius, "Trichome-specific expression of amorpha-4,11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L., as reported by a promoter-GUS fusion," American Journal of Plant Sciences, vol. 2, pp. 619-628, 2011.
20. Y. Wang, K. Yang, F. Jing et al., "Cloning and characterization of trichome-specific promoter of cpr71av1 gene involved in artemisinin biosynthesis in Artemisia annua L," Molecular Biology, vol. 45, no. 5, pp. 751-758, 2011.
21. W. Jiang, X. Lu, B. Qiu et al., "Molecular cloning and characterization of a trichome-specific promoter of artemisinic aldehyde 11(13) reductase (DBR2) in Artemisia annua," Plant Molecular Biology Reporter, vol. 32, no. 1, pp. 82-91, 2014.
22. K. Yang, R. S. Monafared, H. Wang, A. Lundgren, and P. E. Brodelius, "The activity of the artemisinic aldehyde 11(13) reductase promoter is important for artemisinin yield in different chemotypes of Artemisia annua L.," PlantMolecular Biology, vol. 88, no. 4, pp. 325-340, 2015.
23. P. S. Covello, "Making artemisinin," Phytochemistry, vol. 69, no. 17, pp. 2881-2885, 2008.
24. M. Z. Abdin, M. Israr, R. U. Rehman, and S. K. Jain, "Artemisinin, a novel antimalarial drug: biochemical and molecular approaches for enhanced production," Planta Medica, vol. 69, no. 4, pp. 289-299, 2003.
25. S. Aquil, A. M. Husaini,M. Z. Abdin, and G. M. Rather, "Overexpression of the HMG-CoA reductase gene leads to enhanced artemisinin biosynthesis in transgenic Artemisia annua plants," Planta Medica, vol. 75, no. 13, pp. 1453-1458, 2009.
26. T. Nafis,M. Akmal,M. Ramet al., "Enhancement of artemisinin content by constitutive expression of the HMG-CoA reductase gene in high-yielding strain of Artemisia annua L," Plant Biotechnology Reports, vol. 5, no. 1, pp. 53-60, 2011.
27. W. Banyai, C. Kirdmanee, M. Mii, and K. Supaibulwatana, "Overexpression of farnesyl pyrophosphate synthase (FPS) gene affected Artemisinin content and growth of Artemisia annua L," Plant Cell, Tissue and Organ Culture, vol. 103, no. 2,pp. 255-265, 2010.
28. J.-L. Han, B.-Y. Liu, H.-C. Ye, H. Wang, Z.-Q. Li, and G.-F. Li, "Effects of overexpression of the endogenous farnesyl diphosphate synthase on the artemisinin content in Artemisia annua L," Journal of Integrative Plant Biology, vol. 48, no. 4, pp. 482-487, 2006.
29. Y. Yuan,W. Liu, Q. Zhang et al., "Overexpression of artemisinic aldehyde 11 (13) reductase gene-enhanced artemisinin and its relative metabolite biosynthesis in transgenic Artemisia annua L.," Biotechnology and Applied Biochemistry, vol. 62, no. 1, pp. 17-23, 2015.
30. P. Alam and M. Z. Abdin, "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 Reports, vol. 30, no. 10, pp. 1919-1928, 2011.
31. Y. Chen, Q. Shen, Y. Wang et al., "The stacked over-expression of FPS, CYP71AV1 and CPR genes leads to the increase of artemisinin level in Artemisia annua L.," Plant Biotechnology Reports, vol. 7, no. 3, pp. 287-295, 2013.
32. L. Zhang, F. Jing, F. Li et al., "Development of transgenic Artemisia annua (Chinese worm-wood) plants with an enhanced content of artemisinin, an effective anti-malarial drug, by hairpin-RNA-mediated gene silencing," Biotechnology and Applied Biochemistry, vol. 52, no. 3, pp. 199-207, 2009.
33. L.-L. Feng, R.-Y. Yang, X.-Q. Yang, X.-M. Zeng, W.-J. Lu, and Q.-P. Zeng, "Synergistic re-channeling of mevalonate pathway for enhanced artemisinin production in transgenic Artemisia annua," Plant Science, vol. 177, no. 1, pp. 57-67, 2009.
34. J.-L. Chen, H.-M. Fang, Y.-P. Ji et al., "Artemisinin biosynthesis enhancement in transgenic Artemisia annua plants by downregulation of the -caryophyllene synthase gene," Planta Medica, vol. 77, no. 15, pp. 1759-1765, 2011.
35. P. J. Rushton, I. E. Somssich, P. Ringler, andQ. J. Shen, "WRKY transcription factors," Trends in Plant Science, vol. 15, no. 5, pp. 247-258, 2010.
36. T. Eulgem, P. J. Rushton, S. Robatzek, and I. E. Somssich, "The WRKY superfamily of plant transcription factors," Trends in Plant Science, vol. 5, no. 5, pp. 199-206, 2000.
37. B. Ülker and I. E. Somssich, "WRKY transcription factors: from DNA binding towards biological function," Current Opinion in Plant Biology, vol. 7, no. 5, pp. 491-498, 2004.
38. C. Marè, E. Mazzucotelli, C. Crosatti, E. Francia, A. M. Stanca, and L. Cattivelli, "Hv-WRKY38: a new transcription factor involved in cold-and drought-response in barley," PlantMolecular Biology, vol. 55, no. 3, pp. 399-416, 2004.
39. Z. Xie, Z.-L. Zhang, S. Hanzlik, E. Cook, and Q. J. Shen, "Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisicacid-inducible WRKY gene," Plant Molecular Biology, vol. 64, no. 3, pp. 293-303, 2007.
40. X. Zou, D. Neuman, and Q. J. Shen, "Interactions of two transcriptional repressors and two transcriptional activators in modulating gibberellin signaling in aleurone cells," Plant Physiology, vol. 148, no. 1, pp. 176-186, 2008.
41. X. Zou, J. R. Seemann, D. Neuman, and Q. J. Shen, "A WRKY gene from creosote bush encodes an activator of the abscisic acid signaling pathway,"TheJournal of Biological Chemistry, vol. 279, no. 53, pp. 55770-55779, 2004.
42. Y. Qiu and D. Yu, "Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis," Environmental and Experimental Botany, vol. 65, no. 1, pp. 35-47, 2009.
43. X. Wu, Y. Shiroto, S. Kishitani, Y. Ito, and K. Toriyama, "Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter," Plant Cell Reports, vol. 28, no. 1, pp. 21-30, 2009.
44. Y. Jiang and M. K. Deyholos, "Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses," Plant Molecular Biology, vol. 69, no. 1-2, pp. 91-105, 2009.
45. S. Li, Q. Fu, W. Huang, and D. Yu, "Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress," Plant Cell Reports, vol. 28, no. 4, pp. 683-693, 2009.
46. Q.-Y. Zhou, A.-G. Tian, H.-F. Zou et al., "Soybean WRKYtype transcription factor genes,GmWRKY13,GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants," Plant Biotechnology Journal, vol. 6, no. 5, pp. 486-503, 2008.
47. Z. Wang, Y. Zhu, L. Wang et al., "AWRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter," Planta, vol. 230, no. 6,pp. 1155-1166, 2009.
48. X. Ren, Z. Chen, Y. Liu et al., "ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis," Plant Journal, vol. 63, no. 3, pp. 417-429, 2010.
49. S. Vanderauwera, K. Vandenbroucke, A. Inzé et al., "AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis," Proceedings of the NationalAcademy of Sciences of theUnited States ofAmerica, vol. 109, no. 49, pp. 20113-20118, 2012.
50. X. Lu, L. Zhang, F. Zhang et al., "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 Phytologist, vol. 198, no. 4, pp. 1191-1202, 2013.
51. Z.-X. Yu, J.-X. Li, C.-Q. Yang, W.-L. Hu, L.-J. Wang, and X.-Y. Chen, "The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L.," Molecular Plant, vol. 5, no. 2, pp. 353-365, 2012.
52. F. Zhang, X. Fu, Z. Lv et al., "A basic leucine zipper transcription factor, aabzip1, connects abscisic acid signaling with artemisinin biosynthesis in Artemisia annua," Molecular Plant, vol. 8, no. 1, pp. 163-175, 2015.
53. H. Tan, L. Xiao, S. Gao et al., "Trichome and artemisinin regulator 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua," Molecular Plant, vol. 8, no. 9, pp. 1396-1411, 2015.
54. D. Ma, G. Pu, C. Lei et al., "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 and Cell Physiology, vol. 50, no. 12, pp. 2146-2161, 2009.
55. X. Lu, W. Jiang, L. Zhang et al., "Characterization of a novel ERF transcription factor in Artemisia annua and its induction kinetics after hormones and stress treatments," Molecular Biology Reports, vol. 39, no. 10, pp. 9521-9527, 2012.
56. K. J. Livak and T. D. Schmittgen, "Analysis of relative gene expression data using real-time quantitative PCR and the 2-CT method," Methods, vol. 25, no. 4, pp. 402-408, 2001.
57. J.-Y. Zhang, S.-B. He, L. Li, and H.-Q. Yang, "Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll," Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 29, pp. E3015-E3023, 2014.
58. A. Vergauwe, R. Cammaert, D. Vandenberghe et al., "Agrobacterium tumefaciens-mediated transformation of Artemisia annua L. and regeneration of transgenic plants," Plant Cell Reports, vol. 15, no. 12, pp. 929-933, 1996.
59. S. Porebski, L. G. Bailey, and B. R. Baum, "Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components," Plant Molecular Biology Reporter, vol. 15, no. 1, pp. 8-15, 1997.
60. J. Han, H. Wang, A. Lundgren, and P. E. Brodelius, "Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants," Phytochemistry, vol. 102, pp. 89-96, 2014.
61. L. Maes, F. C. W. VanNieuwerburgh, Y. Zhang et al., "Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants," New Phytologist, vol. 189, no. 1,pp. 176-189, 2011.
62. S. S. A. Soetaert, C. M. F. Van Neste, M. L. Vandewoestyne et al., "Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua," BMC Plant Biology, vol. 13, article 220, 2013.
63. L. Olofsson, A. Engström, A. Lundgren, and P. E. Brodelius, "Relative expression of genes of terpenemetabolism in different tissues of Artemisia annua L," BMC Plant Biology, vol. 11, article 45, 2011.