GLANDULAR TRICHOME-SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua

New Phytologist

Volumn 214, Issue 1, 2017, Pages 304-316

  Chen, Minghui ^a   Yan, Tingxiang ^a   Shen, Qian ^a   Lu, Xu ^b   Pan, Qifang ^a   Huang, Youran ^a   Tang, Yueli ^a   Fu, Xueqing ^a   Liu, Meng ^a   Jiang, Weimin ^a   Lv, Zongyou ^a   Shi, Pu ^a   Ma, Ya Nan ^a   Hao, Xiaolong ^a   Zhang, Lida ^a   Li, Ling ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

AaGSW1; abscisic acid (ABA); Artemisia annua; artemisinin biosynthetic pathway; glandular trichome specific; jasmonate (JA)

Indexed keywords

ABSCISIC ACID; ANTIMALARIAL AGENT; BIOASSAY; BIOLOGICAL PRODUCTION; GENE; GENE EXPRESSION; HERB; HORMONE; ORGANIC COMPOUND; PHYSIOLOGICAL RESPONSE; PHYSIOLOGY; TRICHOME;

ARTEMISIA ANNUA;

ABSCISIC ACID; ARTEMISININ; ARTEMISININ DERIVATIVE; BETA GLUCURONIDASE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PLANT PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ANTIBODY SPECIFICITY; ARTEMISIA ANNUA; BIOLOGICAL MODEL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYLOGENY; PLANT GENE; PROMOTER REGION; TRANSGENIC PLANT; TRICHOME;

ABSCISIC ACID; ARTEMISIA ANNUA; ARTEMISININS; BIOSYNTHETIC PATHWAYS; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCURONIDASE; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; OXYLIPINS; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRICHOMES;

EID: 85013993791     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14373     Document Type: Article

References (52)

1. Bouwmeester HJ, Wallaart TE, Janssen MH, van Loo B, Jansen BJ, Posthumus MA, Schmidt CO, De Kraker J-W, König WA, Franssen MC. 1999. Amorpha-4, 11-diene synthase catalyses the first probable step in artemisinin biosynthesis. Phytochemistry 52: 843–854.
2. Brown GD, Sy L-K. 2004. In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60: 1139–1159.
3. Chen X, Liu J, Lin G, Wang A, Wang Z, Lu G. 2013. Overexpression of AtWRKY28 and AtWRKY75 in Arabidopsis enhances resistance to oxalic acid and Sclerotinia sclerotiorum. Plant Cell Reports 32: 1589–1599.
4. Devaiah BN, Karthikeyan AS, Raghothama KG. 2007. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiology 143: 1789–1801.
5. Duke SO, Paul RN. 1993. Development and fine structure of the glandular trichomes of Artemisia annua L. International Journal of Plant Sciences 154: 107–118.
6. Eddy SR. 2011. Accelerated profile HMM searches. PLoS Computational Biology 7: e1002195.
7. Elfawal MA, Towler MJ, Reich NG, Golenbock D, Weathers PJ, Rich SM. 2012. Dried whole plant Artemisia annua as an antimalarial therapy. PLoS One 7: e52746.
8. Elfawal MA, Towler MJ, Reich NG, Weathers PJ, Rich SM. 2015. Dried whole-plant Artemisia annua slows evolution of malaria drug resistance and overcomes resistance to artemisinin. Proceedings of the National Academy of Sciences, USA 112: 821–826.
9. Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de los Santos B, Romero F, Pliego-Alfaro F, Muñoz-Blanco J, Caballero JL. 2009. Evidence for a positive regulatory role of strawberry (Fragaria × ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. Journal of Experimental Botany 60: 3043–3065.
10. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5: 199–206.
11. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44: D279–D285.
12. Gershenzon J, McCaskill D, Rajaonarivony JIM, Mihaliak C, Karp F, Croteau R. 1992. Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Analytical Biochemistry 200: 130–138.
13. Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM et al. 2010. The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327: 328–331.
14. Han JL, Wang HZ, Lundgren A, Brodelius PE. 2014. Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants. Phytochemistry 102: 89–96.
15. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA. 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 1.
16. Ji Y, Xiao J, Shen Y, Ma D, Li Z, Pu G, Li X, Huang L, Liu B, Ye H et al. 2014. Cloning and characterization of AabHLH1, a bHLH transcription factor that positively regulates artemisinin biosynthesis in Artemisia annua. Plant and Cell Physiology 55: 1592–1604.
17. Jiang W, Fu X, Pan Q, Tang Y, Shen Q, Lv Z, Yan T, Shi P, Li L, Zhang L et al. 2016. Overexpression of AaWRKY1 leads to an enhanced content of artemisinin in Artemisia annua. BioMed Research International 2016: 7314971.
18. Jiang W, Lu X, Qiu B, Zhang F, Shen Q, Lv Z, Fu X, Yan T, Gao E, Zhu M et al. 2014. Molecular cloning and characterization of a trichome-specific promoter of artemisinic aldehyde Δ11(13) reductase (DBR2) in Artemisia annua. Plant Molecular Biology Reporter 32: 82–91.
19. Lange BM, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, Croteau R. 2000. Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proceedings of the National Academy of Sciences, USA 97: 2934–2939.
20. Lei L, Li Y, Wang Q, Xu J, Chen Y, Yang H, Ren D. 2014. Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana. New Phytologist 203: 1146–1160.
21. Li Z, Peng J, Wen X, Guo H. 2012. Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. Journal of Integrative Plant Biology 54: 526–539.
22. Lu X, Zhang L, Zhang F, Jiang W, Shen Q, Zhang L, Lv Z, Wang G, Tang K. 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 Phytologist 198: 1191–1202.
23. Ma DM, Pu GB, Lei CY, Ma LQ, Wang HH, Guo YW, Chen JL, Du ZG, Wang H, Li GF 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 and Cell Physiology 50: 2146–2161.
24. Mangan S, Alon U. 2003. Structure and function of the feed-forward loop network motif. Proceedings of the National Academy of Sciences, USA 100: 11980–11985.
25. Mao J, Zhang Y-C, Sang Y, Li Q-H, Yang H-Q. 2005. A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proceedings of the National Academy of Sciences, USA 102: 12270–12275.
26. Mercke P, Bengtsson M, Bouwmeester HJ, Posthumus MA, Brodelius PE. 2000. Molecular cloning, expression, and characterization of amorpha-4, 11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L. Archives of Biochemistry and Biophysics 381: 173–180.
27. Olofsson L, Lundgren A, Brodelius PE. 2012. Trichome isolation with and without fixation using laser microdissection and pressure catapulting followed by RNA amplification: expression of genes of terpene metabolism in apical and sub-apical trichome cells of Artemisia annua L. Plant Science 183: 9–13.
28. Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main A, Eng D et al. 2013. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496: 528–532.
29. Peplow M. 2016. Synthetic malaria drug meets market resistance. Nature 530: 389–390.
30. Phukan UJ, Jeena GS, Shukla RK. 2016. WRKY transcription factors: molecular regulation and stress responses in plants. Frontiers in Plant Science 7: 760.
31. Rishmawi L, Pesch M, Juengst C, Schauss AC, Schrader A, Hülskamp M. 2014. Non-cell-autonomous regulation of root hair patterning genes by WRKY75 in Arabidopsis. Plant Physiology 165: 186–195.
32. Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J. 2006. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940–943.
33. Rushton PJ, Somssich IE, Ringler P, Shen QJ. 2010. WRKY transcription factors. Trends in Plant Science 15: 247–258.
34. Schluttenhofer C, Yuan L. 2015. Regulation of specialized metabolism by WRKY transcription factors. Plant Physiology 167: 295–306.
35. 2 study. Phytochemistry 71: 179–187.
36. Shen Q, Lu X, Yan T, Fu X, Lv Z, Zhang F, Pan Q, Wang G, Sun X, Tang K. 2016a. The jasmonate-responsive AaMYC2 transcription factor positively regulates artemisinin biosynthesis in Artemisia annua. New Phytologist 210: 1269–1281.
37. Shen Q, Yan TX, Fu XQ, Tang KX. 2016b. Transcriptional regulation of artemisinin biosynthesis in Artemisia annua L. Science Bulletin 61: 18–25.
38. Tan H, Xiao L, Gao S, Li Q, Chen J, Xiao Y, Ji Q, Chen R, Chen W, Zhang L. 2015. TRICHOME AND ARTEMISININ REGULATOR 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua. Molecular Plant 8: 1396–1411.
39. Tang K, Shen Q, Yan T, Fu X. 2014. Transgenic approach to increase artemisinin content in Artemisia annua L. Plant Cell Reports 33: 605–615.
40. Teoh KH, Polichuk DR, Reed DW, Covello PS. 2009. Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany-Botanique 87: 635–642.
41. Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS. 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 Letters 580: 1411–1416.
42. Wang H, Han J, Kanagarajan S, Lundgren A, Brodelius P. 2012. 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 81: 119–138.
43. Wang H, Liu W, Qiu F, Chen Y, Zhang F, Lan X, Chen M, Zhang H, Liao Z. 2016. Molecular cloning and characterization of the promoter of aldehyde dehydrogenase gene from Artemisia annua. Biotechnology and Applied Biochemistry doi: 10.1002/bab.1520
44. Wang H, Olofsson L, Lundgren A, Brodelius PE. 2011. 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 2: 619.
45. Weathers PJ, Jordan NJ, Lasin P, Towler MJ. 2014. Simulated digestion of dried leaves of Artemisia annua consumed as a treatment (pACT) for malaria. Journal of Ethnopharmacology 151: 858–863.
46. World Health Organization. 2015. World Malaria Report 2015. [WWW document] http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/ [accessed 9 December 2015].
47. Yang K, Monafared R, Wang H, Lundgren A, Brodelius P. 2015. The activity of the artemisinic aldehyde Δ11(13) reductase promoter is important for artemisinin yield in different chemotypes of Artemisia annua L. Plant Molecular Biology 88: 1–16.
48. Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY. 2011. The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Molecular Plant 5: 353–365.
49. Zhang F, Fu X, Lv Z, Lu X, Shen Q, Zhang L, Zhu M, Wang G, Sun X, Liao Z et al. 2015. A basic leucine zipper transcription factor, AabZIP1, connects abscisic acid signaling with artemisinin biosynthesis in Artemisia annua. Molecular Plant 8: 163–175.
50. Zhang L, Jing FY, Li FP, Li MY, Wang YL, Wang GF, Sun XF, Tang KX. 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. Biotechnology and Applied Biochemistry 52: 199–207.
51. Zhang Y, Teoh KH, Reed DW, Maes L, Goossens A, Olson DJ, Ross AR, Covello PS. 2008. The molecular cloning of artemisinic aldehyde Δ11 (13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. Journal of Biological Chemistry 283: 21501–21508.
52. Zhou M, Memelink J. 2016. Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnology Advances 34: 441–449.