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

Volumn 198, Issue 4, 2013, Pages 1191-1202

  Lu, Xu ^a   Zhang, Ling ^a   Zhang, Fangyuan ^a   Jiang, Weimin ^a   Shen, Qian ^a   Zhang, Lida ^a   Lv, Zongyou ^a   Wang, Guofeng ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Artemisinin; Artemisinin biosynthetic pathway; Dihydroartemisinic acid; Disease resistance to B. cinerea; Secondary metabolism; Trichome specific

Indexed keywords

ARTEMISININ DERIVATIVE; BETA GLUCURONIDASE; DIHYDROARTEMISINIC ACID; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

BIOCHEMISTRY; BIOLOGICAL PRODUCTION; DICOTYLEDON; DISEASE RESISTANCE; FUNCTIONAL ROLE; FUNGAL DISEASE; GENE EXPRESSION; METABOLISM; PHENOTYPE; PLANT PRODUCT; POLYMERASE CHAIN REACTION; TRICHOME;

ANTIBODY SPECIFICITY; ARTEMISIA ANNUA; ARTICLE; BIOSYNTHESIS; BOTRYTIS; CELL FRACTIONATION; CELL NUCLEUS; CHEMISTRY; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ARTEMISIA ANNUA; ARTEMISININS; BIOSYNTHETIC PATHWAYS; BOTRYTIS; CELL NUCLEUS; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUCURONIDASE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS;

AMORPHA; ARABIDOPSIS THALIANA; ARTEMISIA ANNUA; BOTRYOTINIA FUCKELIANA;

EID: 84877622109     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12207     Document Type: Article

References (38)

1. Agarwal PK, Agarwal P, Reddy MK, Sopory SK. 2006. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports 25: 1263-1274.
2. Berrocal-Lobo M, Molina A, Solano R. 2002. Constitutive expression of ETHYLENE-RESPONSE FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant Journal 29: 23-32.
3. Bouwmeester HJ, Wallaart TE, Janssen MH, van Loo B, Jansen BJ, Posthumus MA, Schmidt CO, De Kraker JW, Konig WA, Franssen MC. 1999. Amorpha-4, 11-diene synthase catalyses the first probable step in artemisinin biosynthesis. Phytochemistry 52: 843-854.
4. Brown GD, Sy LK. 2004. In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60: 1139-1159.
5. Brown GD, Sy LK. 2007. In vivo transformations of artemisinic acid in Artemisia annua plants. Tetrahedron 63: 9548-9566.
6. Efferth T. 2007. Antiplasmodial and antitumor activity of artemisinin from bench to bedside. Planta Medica 73: 299-309.
7. Efferth T, Romero MR, Wolf DG, Stamminger T, Marin JJG, Marschall M. 2008. The antiviral activities of artemisinin and artesunate. Clinical Infectious Diseases 47: 804-811.
8. Gao QM, Venugopal S, Navarre D, Kachroo A. 2011. Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiology 155: 464-476.
9. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6: 3901-3907.
10. Kumar S, Tamura K, Jakobsen IB, Nei M. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244-1245.
11. Levin DA. 1973. The role of trichomes in plant defense. Quarterly Review of Biology 48: 3-15.
12. Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R. 2003. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165-178.
13. Lu X, Jiang WM, Zhang L, Zhang FY, Shen Q, Wang T, Chen YF, Wu SY, Lv ZY, Gao ED et al. 2012. Characterization of a novel ERF transcription factor in Artemisia annua and its induction kinetics after hormones and stress treatments. Molecular Biology Reports 39: 9521-9527.
14. 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.
15. Olofsson L, Engström A, Lundgren A, Brodelius PE. 2011. Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biology 11: 45.
16. 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.
17. Olsson ME, Olofsson LM, Lindahl AL, Lundgren A, Brodelius M, Brodelius PE. 2009. Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70: 1123-1128.
18. Reymond P, Farmer EE. 1998. Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology 1: 404-411.
19. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J et al. 2006. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940-943.
20. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
21. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K. 2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochemical and Biophysical Research Communications 290: 998-1009.
22. Schilmiller AL, Last RL, Pichersky E. 2008. Harnessing plant trichome biochemistry for the production of useful compounds. Plant Journal 54: 702-711.
23. Solano R, Stepanova A, Chao QM, Ecker JR. 1998. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes and Development 12: 3703-3714.
24. Teoh KH, Polichuk DR, Reed DW, Covello PS. 2009. Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany 87: 635-642.
25. 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.
26. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
27. Van der Fits L, Memelink J. 2000. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289: 295-297.
28. Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant Journal 33: 949-956.
29. Wallaart TE, Pras N, Quax WJ. 1999. Isolation and identification of dihydroartemisinic acid hydroperoxide from Artemisia annua: a novel biosynthetic precursor of artemisinin. Journal of Natural Products 62: 430-433.
30. Wang HZ, Han JL, Kanagarajan S, Lundgren A, Brodelius PE. 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 Molecular Biology 81: 119-138.
31. Wang HZ, 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: 619-628.
32. Weathers PJ, Arsenault PR, Covello PS, McMickle A, Teoh KH, Reed DW. 2011. Artemisinin production in Artemisia annua: studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochemistry Reviews 10: 173-183.
33. Weathers PJ, Elkholy S, Wobbe KK. 2006. Artemisinin: the biosynthetic pathway and its regulation in Artemisia annua, a terpenoid-rich species. In Vitro Cellular and Developmental Biology-Plant 42: 309-317.
34. Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY. 2012. The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Molecular Plant 5: 353-365.
35. 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.
36. Zhang L, Lu X, Shen Q, Chen YF, Wang T, Zhang FY, Wu SY, Jiang WM, Liu P, Zhang LD 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 Molecular Biology Reporter 4: 838-847.
37. Zhang X, Henriques R, Lin SS, Niu QW, Chua NH. 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1: 641-646.
38. 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.