The DOI matches its Crossref record; 27 of the 27 references it cites were found in a registry or an index.
Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L.
Abstract
A method based on the laser microdissection pressure catapulting technique has been developed for isolation of whole intact cells. Using a modified tissue preparation method, one outer pair of apical cells and two pairs of sub-apical, chloroplast-containing cells, were isolated from glandular secretory trichomes of Artemisia annua. A. annua is the source of the widely used antimalarial drug artemisinin. The biosynthesis of artemisinin has been proposed to be located to the glandular trichomes. The first committed steps in the conversion of FPP to artemisinin are conducted by amorpha-4,11-diene synthase, amorpha-4,11-diene hydroxylase, a cytochrome P450 monooxygenase (CYP71AV1) and artemisinic aldehyde Delta11(13) reductase. The expression of the three biosynthetic enzymes in the different cell types has been studied. In addition, the expression of farnesyldiphosphate synthase producing the precursor of artemisinin has been investigated. Our experiments showed expression of farnesyldiphosphate synthase in apical and sub-apical cells as well as in mesophyl cells while the three enzymes involved in artemisinin biosynthesis were expressed only in the apical cells. Elongation factor 1alpha was used as control and it was expressed in all cell types. We conclude that artemisinin biosynthesis is taking place in the two outer apical cells while the two pairs of chloroplast-containing cells have other functions in the overall metabolism of glandular trichomes.
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In the citing paper
“and the associated genes have been shown to be highly expressed in both the apical and sub-apical cells of the glandular secretory trichomes (3, 16)”
From Artemisia annua mutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism (2016) · cites this paper as [3]
In the citing paper
“The biosynthesis of artemisinin mainly occurs inside the 10-celled structures called glandular trichomes, present in the aerial parts of the plant.”
From Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches (2021) · cites this paper as Olsson et al. 2009
In the citing paper
“Artemisia ketone (276) is formed by a non-standard “head-to-middle” condensation of DMAPP [104,122,123,124,125,126], which is thought to proceed as shown in Scheme 2 via chrysanthemyl pyrophosphate, an intermediate containing a three-membered ring.”
From The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao) (2010) · cites this paper as [104]
In the citing paper
“indeed, it has recently been concluded that artemisinin biosynthesis occurs in the two outer apical cells of the glandular secretory trichomes [104]”
From The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao) (2010) · cites this paper as [104]
Citations
Cites
Qinghaosu (Artemisinin): The Price of Success
White, N. J. (2008) · Science · doi:10.1126/science.1155165 · Cited by 954
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Gang, D. R., Wang, J., Dudareva, N., Nam, K. H., Simon, J. E., Lewinsohn, E., & Pichersky, E. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.125.2.539 · Cited by 506
Harnessing plant trichome biochemistry for the production of useful compounds
Schilmiller, A. L., Last, R. L., & Pichersky, E. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03432.x · Cited by 439
Teoh, K. H., Polichuk, D. R., Reed, D. W., Nowak, G., & Covello, P. S. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.01.065 · Cited by 409
Artemisinin drugs in the treatment of malaria: from medicinal herb to registered medication
van Agtmael, M. A. (1999) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(99)01302-4 · Cited by 351
Zhang, Y., Teoh, K. H., Reed, D. W., Maes, L., Goossens, A., Olson, D. J. H., Ross, A. R. S., & Covello, P. S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803090200 · Cited by 312
Lange, B. M., Wildung, M. R., Stauber, E. J., Sanchez, C., Pouchnik, D. J., & Croteau, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.6.2934 · Cited by 311
Mercke, P., Bengtsson, M., Bouwmeester, H. J., Posthumus, M. A., & Brodelius, P. E. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.1962 · Cited by 283
Self-citationDevelopment and Fine Structure of the Glandular Trichomes of Artemisia annua L.
Duke, S. O., & Paul, R. N. (1993) · International Journal of Plant Sciences · doi:10.1086/297096 · Cited by 276
Duke, M. V., Paul, R. N., Elsohly, H. N., Sturtz, G., & Duke, S. O. (1994) · International Journal of Plant Sciences · doi:10.1086/297173 · Cited by 252
Terpene Biosynthesis in Glandular Trichomes of Hop
Wang, G., Tian, L., Aziz, N., Broun, P., Dai, X., He, J., King, A. J., Zhao, P. X., & Dixon, R. A. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.125187 · Cited by 229
Sapir‐Mir, M., Mett, A., Belausov, E., Tal-Meshulam, S., Frydman, A., Gidoni, D., & Eyal, Y. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.127951 · Cited by 209
Bertea, C. M., Freije, J. R., van der Woude, H., Verstappen, F. W., Perk, L., Marquez, V., De Kraker, J.-W., Posthumus, M. A., Jansen, B. J., de Groot, A., et al. (2005) · Planta Medica · doi:10.1055/s-2005-837749 · Cited by 205
Nagel, J., Culley, L. K., Lu, Y., Liu, E., Matthews, P. D., Stevens, J. F., & Page, J. E. (2008) · The Plant Cell · doi:10.1105/tpc.107.055178 · Cited by 204
Fridman, E., Wang, J., Iijima, Y., Froehlich, J. E., Gang, D. R., Ohlrogge, J. B., & Pichersky, E. (2005) · The Plant Cell · doi:10.1105/tpc.104.029736 · Cited by 189
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Duke, S. O., Vaughn, K. C., Croom, E. M., & ElSohly, H. N. (1987) · Weed Science · doi:10.1017/s0043174500060458 · Cited by 186
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Nelson, T. M., Tausta, S. L., Gandotra, N., & Liu, T. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.56.032604.144138 · Cited by 178
Xie, Z., Kapteyn, J., & Gang, D. R. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03429.x · Cited by 153
Differential accumulation of isoprenoids in glanded and glandless Artemisia annua L
Tellez, M. R., Canel, C., Rimando, A. M., & Duke, S. O. (1999) · Phytochemistry · doi:10.1016/s0031-9422(99)00308-8 · Cited by 148
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Bilyeu, K., Palavalli, L. H., Sleper, D. A., & Beuselinck, P. R. (2003) · Crop Science · doi:10.2135/cropsci2003.1833 · Cited by 144
Bertea, C. M., Voster, A., Verstappen, F. W. A., Maffei, M., Beekwilder, J., & Bouwmeester, H. J. (2006) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2006.02.026 · Cited by 134
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Day, R. C., Grossniklaus, U., & Macknight, R. C. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.06.006 · Cited by 131
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Aziz, N., Paiva, N. L., May, G. D., & Dixon, R. A. (2004) · Planta · doi:10.1007/s00425-004-1424-1 · Cited by 126
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Amme, S., Rutten, T. L. M., Melzer, M., Sonsmann, G., Vissers, J. P. C., Schlesier, B., & Mock, H. (2005) · PROTEOMICS · doi:10.1002/pmic.200401274 · Cited by 91
Nieuwerburgh, F. V., Casteele, S. V., Maes, L., Goossens, A., Inzé, D., Bocxlaer, J. V., & Deforce, D. L. D. (2006) · Journal of Chromatography A · doi:10.1016/j.chroma.2006.03.121 · Cited by 73
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Stich, M., Thalhammer, S., Burgemeister, R., Friedemann, G., Ehnle, S., Lüthy, C., & Schütze, K. (2003) · Pathology - Research and Practice · doi:10.1078/0344-0338-00437 · Cited by 54
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Metadata
- Authors
- Olsson, M. E., Olofsson, L. M., Lindahl, A.-L., Lundgren, A., Brodelius, M., & Brodelius, P. E.
- Corresponding author
- Brodelius, Maria
- Brodelius, Peter E.
- Venue
- Phytochemistry
- Publisher
- Elsevier BV
- Published
- 2009-06
- Volume
- 70
- Issue
- 9
- Pages
- 1123-1128
- ISSN
- 0031-9422 (ISSN-L)
- OpenAlex
- W1967648518
- Cited by
- 241
- References
- 27
- Citations by year
- 2026: 15 · 2025: 7 · 2024: 14 · 2023: 12 · 2022: 15 · 2021: 14 · 2020: 19 · 2019: 17 · 2018: 8 · 2017: 10 · 2016: 17 · 2015: 15 · 2014: 10 · 2013: 12 · 2012: 19
- FWCI
- 7.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Phytochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Crafoordska Stiftelsen
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant tissue culture and regeneration
- Physical Sciences › Chemistry › Organic Chemistry › Sesquiterpenes and Asteraceae Studies
- Keywords
- artemisinin biosynthesis, Artemisia annua, apical cells, amorpha-4,11-diene synthase, CYP71AV1, enzyme localization, laser microdissection, gene expression
- MeSH terms
- Base Sequence, Chloroplasts, Cytochrome P-450 Enzyme System, Gas Chromatography-Mass Spectrometry, Oxidoreductases, Plant Proteins, Plant Leaves, Alkyl and Aryl Transferases, Artemisia annua, Artemisinins
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