Transcriptional regulation of artemisinin biosynthesis in Artemisia annua L.

Science Bulletin

Volumn 61, Issue 1, 2016, Pages 18-25

  Shen, Qian ^a   Yan, Tingxiang ^a   Fu, Xueqing ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Artemisia annua L; Artemisinin; Biosynthesis; Transcription factor

Indexed keywords

EID: 84955639558     PISSN: 20959273     EISSN: 20959281     Source Type: Journal    
DOI: 10.1007/s11434-015-0983-9     Document Type: Review

References (86)

1. Mutabingwa TK (2005) Artemisinin-based combination therapies (ACTS): best hope for malaria treatment but inaccessible to the needy! Acta Trop 95:305–315
2. World Health Organization (2014) World Malaria Report 2014. WHO website. http://www.who.int/malaria/publications/world_malaria_report_2014/en/. Accessed 20 Nov 2015
3. Duffy PE, Mutabingwa TK (2006) Artemisinin combination therapies. Lancet 367:2037–2039
4. Romero MR, Serrano MA, Vallejo M et al (2006) Antiviral effect of artemisinin from Artemisia annua against a model member of the Flaviviridae family, the bovine viral diarrhoea virus (BVDV). Planta Med 72:1169–1174
5. Nam W, Tak J, Ryu JK et al (2007) Effects of artemisinin and its derivatives on growth inhibition and apoptosis of oral cancer cells. Head Neck 29:335–340
6. Efferth T (2006) Molecular pharmacology and pharmacogenomics of artemisinin and its derivatives in cancer cells. Curr Drug Targets 7:407–421
7. Utzinger J, Xiao SH, Tanner M et al (2007) Artemisinins for schistosomiasis and beyond. Curr Opin Invest Drugs (London, England: 2000) 8:105–116
8. Ro DK, Paradise EM, Ouellet M et al (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943
9. Paddon C, Westfall P, Pitera D et al (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496:528–532
10. Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700
11. Yang L, Yang C, Li C et al (2015) Recent advances in biosynthesis of bioactive compounds in traditional Chinese medicinal plants. Sci Bull 61:3–17
12. 2 study. Phytochemistry 71:179–187
13. Mercke P, Bengtsson M, Bouwmeester HJ et al (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
14. Chang YJ, Song SH, Park SH et al (2000) Amorpha-4, 11-diene synthase of Artemisia annua: cDNA isolation and bacterial expression of a terpene synthase involved in artemisinin biosynthesis. Arch Biochem Biophys 383:178–184
15. Teoh KH, Polichuk DR, Reed DW et al (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
16. Zhang Y, Teoh KH, Reed DW et al (2008) The molecular cloning of artemisinic aldehyde Δ11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J Biol Chem 283:21501–21508
17. Teoh KH, Polichuk DR, Reed DW et al (2009) Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany 87:635–642
18. Brown GD, Sy LK (2004) In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60:1139–1159
19. Brown GD, Sy LK (2007) In vivo transformations of artemisinic acid in Artemisia annua plants. Tetrahedron 63:9548–9566
20. Yang CQ, Fang X, Wu XM et al (2012) Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol 54:703–712
21. Patra B, Schluttenhofer C, Wu Y et al (2013) Transcriptional regulation of secondary metabolite biosynthesis in plants. BBA Gene Regul Mech 1829:1236–1247
22. Verpoorte R, Memelink J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13:181–187
23. van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297
24. Van Moerkercke A, Steensma P, Schweizer F et al (2015) The bHLH transcription factor BIS1 controls the iridoid branch of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Proc Natl Acad Sci USA 112:8130–8135
25. Rushton PJ, Somssich IE, Ringler P et al (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
26. Rushton DL, Tripathi P, Rabara RC et al (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11
27. Ma DM, Pu GB, Lei CY 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 Cell Physiol 50:2146–2161
28. Han J, Wang H, Lundgren A et al (2014) Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants. Phytochemistry 102:89–96
29. Licausi F, Ohme-Takagi M, Perata P (2013) APETALA/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649
30. Zhu Z (2014) Molecular basis for jasmonate and ethylene signal interactions in Arabidopsis. J Exp Bot 65:5743–5748
31. Pan Q, Wang Q, Yuan F et al (2012) Overexpression of ORCA3 and G10H in Catharanthus roseus plants regulated alkaloid biosynthesis and metabolism revealed by NMR-metabolomics. PLoS ONE 7:e43038
32. Lu X, Zhang L, Zhang F 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
33. Yu ZX, Li JX, Yang CQ et al (2012) The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant 5:353–365
34. Sakuma Y, Liu Q, Dubouzet JG et al (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009
35. McGrath KC, Dombrecht B, Manners JM et al (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959
36. Olsson ME, Olofsson LM, Lindahl A-L et al (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70:1123–1128
37. Maes L, Van Nieuwerburgh FC, Zhang Y et al (2010) Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 189:176–189
38. Yang CX, Li HX, Zhang JH et al (2011) A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci USA 108:11836–11841
39. Kjaer A, Grevsen K, Jensen M (2014) Trichomes in Artemisia annua: initiation, development, maturation and the possibilities to influence these factors. In: Aftab T (ed) A. annua—pharmacology biotechnology, 1st edn. Springer, Berlin, pp 113–123
40. Yang CX, Ye ZB (2013) Trichomes as models for studying plant cell differentiation. Cell Mol Life Sci 70:1937–1948
41. Kannangara R, Branigan C, Liu Y et al (2007) The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19:1278–1294
42. Oshima Y, Shikata M, Koyama T et al (2013) MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25:1609–1624
43. Borisjuk N, Hrmova M, Lopato S (2014) Transcriptional regulation of cuticle biosynthesis. Biotechnol Adv 32:526–540
44. Tan H, Xiao L, Gao S et al (2015) TRICHOME AND ARTEMISININ REGULATOR 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua L. Mol Plant 8:1396–1411
45. Jakoby M, Weisshaar B, Dröge-Laser W et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111
46. Wang J, Zhou J, Zhang B et al (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on Sorghum. J Integr Plant Biol 53:212–231
47. Baloglu MC, Eldem V, Hajyzadeh M et al (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE 9:e96014
48. Silveira AB, Gauer L, Tomaz JP et al (2007) The Arabidopsis AtbZIP9 protein fused to the VP16 transcriptional activation domain alters leaf and vascular development. Plant Sci 172:1148–1156
49. Baena-González E, Rolland F, Thevelein JM et al (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942
50. Chen D, Xu G, Tang W et al (2013) Antagonistic basic helix–loop–helix/bZIP transcription factors form transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25:1657–1673
51. Ying S, Zhang D-F, Fu J et al (2012) Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235:253–266
52. Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Bio 21:133–139
53. Choi HI, Hong JH, Ha JO et al (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730
54. Jing F, Zhang L, Li M et al (2009) Abscisic acid (ABA) treatment increases artemisinin content in Artemisia annua by enhancing the expression of genes in artemisinin biosynthetic pathway. Biologia 64:319–323
55. Zhang F, Fu X, Lv Z 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
56. Carretero-Paulet L, Galstyan A, Roig-Villanova I et al (2010) Genome-Wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, Poplar, Rice, Moss, and Algae. Plant Physiol 153:1398–1412
57. Li XX, Duan XP, Jiang HX et al (2006) Genome-wide analysis of basic/helix–loop–helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184
58. Atchley WR, Fitch WM (1997) A natural classification of the basic helix–loop–helix class of transcription factors. Proc Natl Acad Sci USA 94:5172–5176
59. Atchley WR, Wollenberg KR, Fitch WM et al (2000) Correlations among amino acid sites in bHLH protein domains: an information theoretic analysis. Mol Biol Evol 17:164–178
60. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770
61. Pires N, Dolan L (2010) Origin and diversification of basic–helix–loop–helix proteins in plants. Mol Biol Evol 27:862–874
62. Castelain M, Le Hir R, Bellini C (2012) The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiol Plantarum 145:450–460
63. Pozo MJ, Van Der Ent S, Van Loon LC et al (2008) Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol 180:511–523
64. Laurie-Berry N, Joardar V, Street IH et al (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact 19:789–800
65. Abe H, Urao T, Ito T et al (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
66. Zhang H, Hedhili S, Montiel G et al (2011) The basic helix–loop–helix transcription factor CrMYC2 controls the jasmonate—responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. Plant J 67:61–71
67. Zhang HB, Bokowiec MT, Rushton PJ et al (2012) Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis. Mol Plant 5:73–84
68. Lorenzo O, Chico JM, Sanchez-Serrano JJ et al (2004) Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950
69. Hong GJ, Xue XY, Mao YB et al (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648
70. Ji Y, Xiao J, Shen Y et al (2014) Cloning and characterization of AabHLH1, a bHLH transcription factor that positively regulates artemisinin biosynthesis in Artemisia annua. Plant Cell Physiol 55:1592–1604
71. Tang KX,Shen Q, Lu X et al (2013) Sweet wormwood MYC2 transcription factor protein coding sequence and applications thereof. China Patent ZL201310413155.3
72. Matas AJ, Yeats TH, Buda GJ et al (2011) Tissue-and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23:3893–3910
73. Soetaert SS, Van Neste CM, Vandewoestyne ML et al (2013) Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua. BMC Plant Biol 13:220
74. Moses T, Pollier J, Shen Q et al (2015) OSC2 and CYP716A14v2 catalyze the biosynthesis of triterpenoids for the cuticle of aerial organs of Artemisia annua. Plant Cell 27:286–301
75. Afrin S, Huang JJ, Luo ZY (2015) JA-mediated transcriptional regulation of secondary metabolism in medicinal plants. Sci Bull 60:1062–1072
76. van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43–53
77. Caretto S, Quarta A, Durante M et al (2011) Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol 13:51–58
78. Lenka SK, Nims NE, Vongpaseuth K et al (2015) Jasmonate-responsive expression of paclitaxel biosynthesis genes in Taxus cuspidata cultured cells is negatively regulated by the bHLH transcription factors TcJAMYC1, TcJAMYC2, and TcJAMYC4. Front Plant Sci 6:115
79. Kim YS, Yeung EC, Hahn EJ et al (2007) Combined effects of phytohormone, indole-3-butyric acid, and methyl jasmonate on root growth and ginsenoside production in adventitious root cultures of Panax ginseng CA Meyer. Biotechnol Lett 29:1789–1792
80. Wu W, Yuan M, Zhang Q et al (2011) Chemotype-dependent metabolic response to methyl jasmonate elicitation in Artemisia annua. Planta Med 77:1048–1053
81. Lu X, Zhang F, Shen Q et al (2014) Overexpression of allene oxide cyclase improves the biosynthesis of artemisinin in Artemisia annua L. PLoS ONE 9:e91741
82. Aftab T, Khan MMA, Idrees M et al (2011) Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma 248:601–612
83. Qi TC, Song SS, Ren QC et al (2011) The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23:1795–1814
84. Zhao L, Gao L, Wang H et al (2013) The R2R3-MYB, bHLH, WD40, and related transcription factors in flavonoid biosynthesis. Funct Integr Genomic 13:75–98
85. Weathers P, Reed K, Hassanali A et al (2014) Whole plant approaches to therapeutic use of Artemisia annua L. (Asteraceae). In: Aftab T (ed) A. annua—pharmacology biotechnology, 1st edn. Springer, Berlin, pp 51–74
86. Elfawal MA, Towler MJ, Reich NG et al (2015) Dried whole-plant Artemisia annua slows evolution of malaria drug resistance and overcomes resistance to artemisinin. Proc Natl Acad Sci USA 112:821–826