Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Soetaert, Sandra S A ^a   Van Neste, Christophe M F ^a   Vandewoestyne, Mado L ^a   Head, Steven R ^b   Goossens, Alain ^a   Van Nieuwerburgh, Filip C W ^a   Deforce, Dieter L D ^a  

^a GHENT UNIVERSITY   (Belgium)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Artemisia annua; Artemisinin; Filamentous trichomes; Glandular trichomes; Laser microdissection pressure catapulting; Lipid biosynthesis; MEP pathway; Mevalonate pathway; RNASeq; Terpene biosynthesis

Indexed keywords

ARTEMISIA ANNUA;

ARTEMISIA ANNUA; ARTICLE; CYTOLOGY; GENE EXPRESSION PROFILING; TRICHOME;

ARTEMISIA ANNUA; GENE EXPRESSION PROFILING; TRICHOMES;

EID: 84890454272     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-220     Document Type: Article

References (67)

1. WHO World Malaria Report 2011, Geneva: World Health Organization, WHO.
2. Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM, et al. The genetic map of Artemisia annua L identifies Loci affecting yield of the antimalarial drug artemisinin. Science 2010, 327(5963):328-331. 10.1126/science.1182612, 20075252.
3. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440(7086):940-943. 10.1038/nature04640, 16612385.
4. Levesque F, Seeberger PH. Continuous-flow synthesis of the anti-malaria drug artemisinin. Angew Chem-Int Edit 2012, 51(7):1706-1709.
5. Duke MV, Paul RN, Elsohly HN, Sturtz G, Duke SO. Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Int J Plant Sci 1994, 155(3):365-372.
6. Ferreira JFS, Janick J. Floral morphology of Artemisia annua with special reference to trichomes. Int J Plant Sci 1995, 156(6):807-815.
7. Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS. 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 2006, 580(5):1411-1416. 10.1016/j.febslet.2006.01.065, 16458889.
8. Teoh KH, Polichuk DR, Reed DW, Covello PS. Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany 2009, 87(6):635-642.
9. Zhang Y, Teoh KH, Reed DW, Maes L, Goossens A, Olson DJH, Ross ARS, Covello PS. The molecular cloning of artemisinic aldehyde Delta 11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J Biol Chem 2008, 283(31):21501-21508. 10.1074/jbc.M803090200, 18495659.
10. Polichuk D, Teoh KH, Zhang Y, Ellens KW RD, Covello PS. Nucleotide sequence encoding an alcohol dehydrogenease from Artemisia annua and uses thereof 2010, Patent No. WO/2010/012074, February 4th.
11. Brown GD, Sy LK. In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 2004, 60(5):1139-1159.
12. Wang W, Wang YJ, Zhang Q, Qi Y, Guo DJ. Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. Bmc Genomics 2009, 10:465. 10.1186/1471-2164-10-465, 2763888, 19818120.
13. Wagner GJ. Secreting glandular trichomes: more than just hairs. Plant Physiol 1991, 96(3):675-679. 10.1104/pp.96.3.675, 1080829, 16668241.
14. Levin DA. The role of trichomes in plant defence. Q Rev Plant Biol 1973, 48(1):3-15.
15. Mauricio R, Rausher MD. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 1997, 51(5):1435-1444.
16. Victorio CP, Moreira CB, Souza MD, Sato A, Arruda RDD. Secretory cavities and volatiles of Myrrhinium atropurpureum Schott var. atropurpureum (Myrtaceae): an endemic species collected in the Restingas of Rio de Janeiro, Brazil. Nat Prod Commun 2011, 6(7):1045-1050.
17. Porto NM, De Figueiredo R, Oliveira AFM, Agra MD. Leaf epidermal characteristics of Cissampelos L. (Menispermaceae) species from Northeastern Brazil. Microsc Res Tech 2011, 74(4):370-376.
18. Bhatt A, Naidoo Y, Nicholas A. The foliar trichomes of Hypoestes aristata (Vahl) Sol. ex Roem. & Schult var aristata (Acanthaceae) a widespread medicinal plant species in tropical sub-Saharan Africa: with comments on its possible phylogenetic significance. Biol Res 2010, 43(4):403-409. 10.4067/S0716-97602010000400004, 21526266.
19. Duarte MR, Lopes JF. Leaf and stem morphoanatomy of Petiveria alliacea. Fitoterapia 2005, 76(7-8):599-607.
20. Bonzani NE, Barboza GE, Bugatti MA, Espinar LA. Morpho-histological studies in the aromatic species of Chenopodium from Argentina. Fitoterapia 2003, 74(3):207-225. 10.1016/S0367-326X(03)00024-8, 12727484.
21. Wagner GJ, Wang E, Shepherd RW. New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 2004, 93(1):3-11. 10.1093/aob/mch011, 14678941.
22. Maes L, Van Nieuwerburgh FCW, Zhang YS, Reed DW, Pollier J, Casteele S, Inze D, Covello PS, Deforce DLD, Goossens A. Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 2011, 189(1):176-189. 10.1111/j.1469-8137.2010.03466.x, 20874804.
23. Olofsson L, Lundgren A, Brodelius PE. 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 Sci 2012, 183:9-13.
24. Delabays N, Simonnet X, Gaudin M. The genetics of artemisinin content in Artemisia annua L. and the breeding of high yielding cultivars. Curr Med Chem 2001, 8(15)):1795-1801.
25. Ferreira JFS, Laughlin JC, Delabays N, Magalhaes PM. Cultivation and genetics of Artemisia annua L. for increased production of the antimalarial artemisinin. Plant Genet Resour-Characterization Util 2005, 3(2):206-229.
26. WHO Meeting on the production of artemisinin and artemisinin-based combination therapies; Tanzania 2005, Geneva, Switzerland: World Health Organization, WHO.
27. Van Nieuwerburgh F, Soetaert S, Podshivalova K, Ay-Lin Wang E, Schaffer L, Deforce D, Salomon DR, Head SR, Ordoukhanian P. Quantitative bias in Illumina TruSeq and a novel post amplification barcoding strategy for multiplexed DNA and small RNA deep sequencing. PLoS One 2011, 6(10):e26969. 10.1371/journal.pone.0026969, 3203936, 22046424.
28. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007, 8(2):R19. 10.1186/gb-2007-8-2-r19, 1852402, 17291332.
29. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 2005, 139(1):5-17. 10.1104/pp.105.063743, 1203353, 16166256.
30. Olofsson L, Engstrom A, Lundgren A, Brodelius PE. Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 2011, 11:45. 10.1186/1471-2229-11-45, 3063820, 21388533.
31. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. Bmc Bioinformatics 2012, 13:13. 10.1186/1471-2105-13-13, 3292499, 22264315.
32. Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A 2011, 108(4):1513-1518. 10.1073/pnas.1017351108, 3029755, 21187386.
33. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652. 10.1038/nbt.1883, 3571712, 21572440.
34. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36(10):3420-3435. 10.1093/nar/gkn176, 2425479, 18445632.
35. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
36. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. Bmc Bioinformatics 2011, 12:323. 10.1186/1471-2105-12-323, 3163565, 21816040.
37. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
38. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11(3):R25. 10.1186/gb-2010-11-3-r25, 2864565, 20196867.
39. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37(6):914-939. 10.1111/j.1365-313X.2004.02016.x, 14996223.
40. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35(21):7188-7196. 10.1093/nar/gkm864, 2175337, 17947321.
41. Chan PP, Lowe TM. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 2009, 37:D93-D97. 10.1093/nar/gkn787, 2686519, 18984615.
42. Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chetelat A, Haupt I, Kennerley BJ, Hodgens C, et al. A regulatory network for coordinated flower maturation. PLoS Genet 2012, 8(2):17.
43. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 2005, 132(18):4107-4118. 10.1242/dev.01955, 16107481.
44. Ram M, Khan MA, Jha P, Khan S, Kiran U, Ahmad MM, Javed S, Abdin MZ. HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants. Acta Physiol Plant 2010, 32(5):859-866.
45. Aquil S, Husaini AM, Abdin MZ, Rather GM. Overexpression of the HMG-CoA reductase gene leads to enhanced artemisinin biosynthesis in transgenic Artemisia annua plants. Planta Med 2009, 75(13):1453-1458. 10.1055/s-0029-1185775, 19551613.
46. Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, et al. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiol 2005, 138(3):1195-1204. 10.1104/pp.105.060459, 1176394, 16009995.
47. Bouwmeester HJ, Wallaart TE, Janssen MHA, van Loo B, Jansen BJM, Posthumus MA, Schmidt CO, De Kraker JW, Konig WA, Franssen MCR. Amorpha-4,11-diene synthase catalyses the first probable step in artemisinin biosynthesis. Phytochemistry 1999, 52(5):843-854. 10.1016/S0031-9422(99)00206-X, 10626375.
48. Ryden AM, Ruyter-Spira C, Quax WJ, Osada H, Muranaka T, Kayser O, Bouwmeester H. The molecular cloning of dihydroartemisinic aldehyde reductase and its implication in artemisinin biosynthesis in Artemisia annua. Planta Med 2010, 76(15):1778-1783. 10.1055/s-0030-1249930, 20486073.
49. Bertea CM, Freije JR, van der Woude H, Verstappen FWA, Perk L, Marquez V, De Kraker JW, Posthumus MA, Jansen BJM, de Groot A, et al. Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. Planta Med 2005, 71(1):40-47. 10.1055/s-2005-837749, 15678372.
50. Covello PS, Teoh KH, Polichuk DR, Reed DW, Nowak G. Functional genomics and the biosynthesis of artemisinin 2007, 1864-1871. Oxford, MS: Pergamon-Elsevier Science Ltd, Annual Meeting of the Phytochemical-Society-of-North-American: 2006 2007.
51. Van Nieuwerburgh FCW, Casteele SRV, Maes L, Goossens A, Inze D, Van Bocxlaer J, Deforce DLD. Quantitation of artemisinin and its biosynthetic precursors in Artemisia annua L. by high performance liquid chromatography - electrospray quadrupole time-of-flight tandem mass spectrometry. J Chromatogr A 2006, 1118(2):180-187. 10.1016/j.chroma.2006.03.121, 16650427.
52. Wang H, Olofsson L, Lundgren A, Brodelius PE. 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. J Plant Sci 2011, 2(4):619-628.
53. Cabello-Hurtado F, Batard Y, Salaun JP, Durst F, Pinot F, Werck-Reichhart D. Cloning, expression in yeast, and functional characterization of CYP81B1, a plant cytochrome P450 that catalyzes in-chain hydroxylation of fatty acids. J Biol Chem 1998, 273(13):7260-7267. 10.1074/jbc.273.13.7260, 9516419.
54. Salaun JP, Weissbart D, Durst F, Pflieger P, Mioskowski C. Epoxidation of cis-delta-9 and trans-delta-9-unsaturated lauric acids by a cytochrome P-450-dependent system from higher-plant microsomes. Febs Letters 1989, 246(1-2):120-126.
55. Tholl D, Sohrabi R, Huh JH, Lee S. The biochemistry of homoterpenes - common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 2011, 72(13):1635-1646. 10.1016/j.phytochem.2011.01.019, 21334702.
56. Lee S, Badieyan S, Bevan DR, Herde M, Gatz C, Tholl D. Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc Natl Acad Sci U S A 2010, 107(49):21205-21210. 10.1073/pnas.1009975107, 3000306, 21088219.
57. Donath J, Boland W. Biosynthesis of acyclic homoterpenes in higher-plants parallels steroid-hormone metabolism. J Plant Physiol 1994, 143(4-5):473-478.
58. Misra A, Chanotiya CS, Gupta MM, Dwivedi UN, Shasany AK. Characterization of cytochrome P450 monooxygenases isolated from trichome enriched fraction of Artemisia annua L. leaf. Gene 2012, 510(2):193-201. 10.1016/j.gene.2012.09.015, 22986332.
59. Tellez MR, Canel C, Rimando AM, Duke SO. Differential accumulation of isoprenoids in glanded and glandless Artemisia annua L. Phytochemistry 1999, 52(6):1035-1040.
60. Nguyen DT, Gopfert JC, Ikezawa N, MacNevin G, Kathiresan M, Conrad J, Spring O, Ro DK. Biochemical conservation and evolution of germacrene a oxidase in Asteraceae. J Biol Chem 2010, 285(22):16588-16598. 10.1074/jbc.M110.111757, 2878029, 20351109.
61. Hua L, Matsuda SPT. The molecular cloning of 8-epicedrol synthase from Artemisia annua. Arch Biochem Biophys 1999, 369(2):208-212. 10.1006/abbi.1999.1357, 10486139.
62. Mercke P, Crock J, Croteau R, Brodelius PE. Cloning, expression, and characterization of epi-cedrol synthase, a sesquiterpene cyclase from Artemisia annua L. Arch Biochem Biophys 1999, 369(2):213-222. 10.1006/abbi.1999.1358, 10486140.
63. Kirby J, Romanini DW, Paradise EM, Keasling JD. Engineering triterpene production in Saccharomyces cerevisiae-beta-amyrin synthase from Artemisia annua. Febs J 2008, 275(8):1852-1859. 10.1111/j.1742-4658.2008.06343.x, 18336574.
64. Samuels L, Kunst L, Jetter R. Sealing plant surfaces: Cuticular wax formation by epidermal cells 2008, 683-707. Palo Alto: Annual Reviews, Annual Review of Plant Biology.
65. Kunst L, Samuels L. Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 2009, 12(6):721-727. 10.1016/j.pbi.2009.09.009, 19864175.
66. Bao XM, Katz S, Pollard M, Ohlrogge J. Carbocyclic fatty acids in plants: Biochemical and molecular genetic characterization of cyclopropane fatty acid synthesis of Sterculia foetida. Proc Natl Acad Sci U S A 2002, 99(10):7172-7177. 10.1073/pnas.092152999, 124547, 11997456.
67. Yu XH, Rawat R, Shanklin J. Characterization and analysis of the cotton cyclopropane fatty acid synthase family and their contribution to cyclopropane fatty acid synthesis. BMC Plant Biol 2011, 11:97. 10.1186/1471-2229-11-97, 3132707, 21612656.