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

Volumn 30, Issue 4, 2012, Pages 838-847

  Zhang, Ling ^a   Lu, Xu ^a   Shen, Qian ^a   Chen, Yunfei ^a   Wang, Tao ^a   Zhang, Fangyuan ^a   Wu, Shaoyan ^a   Jiang, Weimin ^a   Liu, Pin ^a   Zhang, Lida ^a   Wang, Yueyue ^a   Tang, Kexuan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

ABCG transporter; ADS; Artemisia annua; Artemisinin; CYP71AV1; Trichome cuticle

Indexed keywords

AMORPHA; ARTEMISIA ANNUA;

EID: 84862490324     PISSN: 07359640     EISSN: 15729818     Source Type: Journal    
DOI: 10.1007/s11105-011-0400-8     Document Type: Article

References (50)

1. Arsenault PR, Vail D, Wobbe KK, Erickson K, Weathers PJ (2010) Reproductive development modulates gene expression and metabolite levels with possible feedback inhibition of artemisinin in Artemisia annua. Plant Physiol 154: 958-968.
2. Arsenault PR, Wobbe KK, Weathers PJ (2008) Recent advances in artemisinin production through heterologous expression. Curr Med Chem 15: 2886-2896.
3. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yephremov A, Samuels L (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52: 485-498.
4. Brown GD, Sy L-K (2004) In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60: 1139-1159.
5. Brown GD, Sy L-K (2007) In vivo transformations of artemisinic acid in Artemisia annua plants. Tetrahedron 63: 9548-9566.
6. Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133: 1272-1284.
7. Chang MCY, Eachus RA, Trieu W, Ro D-K, Keasling JD (2007) Engineering Escherichia coli for production of functionalized terpenoids using plant p450s. Nat Chem Biol 3: 274-277.
8. Covello PS (2008) Making artemisinin. Phytochemistry 69: 2881-2885.
9. Dai X, Wang G, Yang DS, Tang Y, Broun P, Marks MD, Sumner LW, Dixon RA, Zhao PX (2010) Trichome: a comparative omics database for plant trichomes. Plant Physiol 152: 44-54.
10. Demetriou K, Kapazoglou A, Bladenopoulos K, Tsaftaris AS (2010) Epigenetic chromatin modifiers in barley: II. Characterization and expression analysis of the HDA1 family of barley histone deacetylases during development and in response to jasmonic acid. Plant Mol Biol Rep 28: 9-21.
11. Duke M, Paul R, Elsohly H, Sturtz G, Duke S (1994) Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Int J Plant Sci 155: 365-372.
12. Efferth T (2007) Willmar Schwabe Award 2006: antiplasmodial and antitumor activity of artemisinin-from bench to bedside. Planta Med 73: 299-309.
13. Efferth T, Romero MR, Wolf DG, Stamminger T, Marin JJG, Marschall M (2008) The antiviral activities of artemisinin and artesunate. Clin Infect Dis 47: 804-811.
14. Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM, Larson TR, Li Y, Pawson T, Penfield T, Rae AM, Rathbone DA, Reid S, Ross J, Smallwood MF, Segura V, Townsend T, Vyas D, Winzer T, Bowles D (2010) The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327: 328-331.
15. Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095-1107.
16. Kim D-W, Kim RN, Choi S-H, Kim D-W, Nam S-H, Choi H-S, Koh HD, Kim A, Chae S-H, Ahn JC, Kang A, Park H-S (2011) EST analysis predicts putatively causative genes underlying the pharmaceutical application of Glycyrrhiza uralensis Fisch. Plant Mol Biol Rep 29: 814-824.
17. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(t)) method. Methods 25: 402-408.
18. Lommen WJM, Elzinga S, Verstappen FWA, Bouwmeester HJ (2007) Artemisinin and sesquiterpene precursors in dead and green leaves of Artemisia annua L. crops. Planta Med 73: 1133-1139.
19. Lommen WJM, Schenk E, Bouwmeester HJ, Verstappen FWA (2006) Trichome dynamics and artemisinin accumulation during development and senescence of Artemisia annua leaves. Planta Med 72: 336-345.
20. Lu X, Lin X, Shen Q, Zhang F, Wang Y, Chen Y, Wang T, Wu S, Tang K (2011) Characterization of the jasmonate biosynthetic gene allene oxide cyclase in Artemisia annua L., source of the antimalarial drug artemisinin. Plant Mol Biol Rep 29: 489-497.
21. Maes L, van Nieuwerburgh FCW, Zhang Y, Reed DW, Pollier J, Vande Casteele SRF, Inzé D, Covello PS, Deforce DLD, Goossens A (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.
22. 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. Arch Biochem Biophys 381: 173-180.
23. Milhous WK, Weina PJ (2010) Plant science. The botanical solution for malaria Science 327: 279-280.
24. Oksman-Caldentey K-M, Inzé D (2004) Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends Plant Sci 9: 433-440.
25. 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 Biol 11: 45. doi: 10. 1186/1471-2229-11-45.
26. Olsson ME, Olofsson LM, Lindahl A-L, 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.
27. Panikashvili D, Aharoni A (2008) ABC-type transporters and cuticle assembly: linking function to polarity in epidermis cells. Plant Signal Behav 3: 806-809.
28. Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A (2010) The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant 3: 563-575.
29. Panikashvili D, Shi JX, Schreiber L, Aharoni A (2011) The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol 190(1): 113-124. doi: 10. 1111/j. 1469-8137. 2010. 03608. x.
30. Pighin JA (2004) Plant cuticular lipid export requires an ABC transporter. Science 306: 702-704.
31. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58: 347-375.
32. Ro D-K, Ouellet M, Paradise EM, Burd H, Eng D, Paddon CJ, Newman JD, Keasling JD (2008) Induction of multiple pleiotropic drug resistance genes in yeast engineered to produce an increased level of anti-malarial drug precursor, artemisinic acid. BMC Biotechnol 8: 83. doi: 10. 1186/1472-6750-8-83.
33. Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940-943.
34. Sánchez-Fernández R, Davies TG, Coleman JO, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276: 30231-44.
35. 2 study. Phytochemistry 71: 179-187.
36. 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.
37. 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 Lett 580: 1411-1416.
38. Tripathy MK, Tyagi W, Goswami M, Kaul T, Singla-Pareek SL, Deswal R, Reddy MK, Sopory SK (2011) Characterization and functional validation of tobacco PLC Delta for abiotic stress tolerance. Plant Mol Biol Rep. doi: 10. 1007/s11105-011-0360-z.
39. Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci 13: 151-159.
40. Wallaart T, van Uden W, Lubberink H, Woerdenbag H, Pras N, Quax W (1999) Isolation and identification of dihydroartemisinic acid from Artemisia annua and its possible role in the biosynthesis of artemisinin. J Nat Prod 62: 430-433.
41. Wallaart TE, Bouwmeester HJ, Hille J, Poppinga L, Maijers NC (2001) Amorpha-4, 11-diene synthase: cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 212: 460-465.
42. Wang W-K, Liu C-C, Chiang T-Y, Chen M-T, Chou C-H, Yeh C-H (2011) Characterization of expressed sequence tags from flower buds of alpine Lilium formosanum using a subtractive cdna library. Plant Mol Biol Rep 29: 88-97.
43. Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8: 301-307.
44. Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580: 1183-1191.
45. Zambounis AG, Kalamaki MS, Tani EE, Paplomatas EJ, Tsaftaris AS (2011) Expression analysis of defense-related genes in cotton (Gossypium hirsutum) after Fusarium oxysporum f. sp. vasinfectum infection and following chemical elicitation using a salicylic acid analog and methyl jasmonate. Plant Mol Biol Rep. doi: 10. 1007/s11105-011-0335-0.
46. Zeng Q, Qiu F, Yuan L (2008) Production of artemisinin by genetically-modified microbes. Biotechnol Lett 30: 581-592.
47. Zhang D, Hu C, Ouyang Y, Yao J (2011a) Construction of a full-length cDNA library and analysis of expressed sequence tags from inflorescence of apomictic sabaigrass (Eulaliopsis binata). Plant Mol Biol Rep. doi: 10. 1007/s11105-011-0316-3.
48. Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011b) Planttfdb 2. 0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39: D1114-1117.
49. Zhang L, Jing F, Li F, Li M, Wang Y, Wang G, Sun X, Tang K (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. Biotechnol Appl Biochem 52: 199-207.
50. Zhang Y, Teoh KH, Reed DW, Maes L, Goossens A, Olson DJH, Ross ARS, Covello PS (2008) The molecular cloning of artemisinic aldehyde delta11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J Biol Chem 283: 21501-21508.