Cloning and Functional Characterization of a β-Pinene Synthase from Artemisia annua That Shows a Circadian Pattern of Expression
Open accessAbstract
Artemisia annua plants produce a broad range of volatile compounds, including monoterpenes, which contribute to the characteristic fragrance of this medicinal species. A cDNA clone, QH6, contained an open reading frame encoding a 582-amino acid protein that showed high sequence identity to plant monoterpene synthases. The prokaryotically expressed QH6 fusion protein converted geranyl diphosphate to (-)-beta-pinene and (-)-alpha-pinene in a 94:6 ratio. QH6 was predominantly expressed in juvenile leaves 2 weeks postsprouting. QH6 transcript levels were transiently reduced following mechanical wounding or fungal elicitor treatment, suggesting that this gene is not directly involved in defense reaction induced by either of these treatments. Under a photoperiod of 12 h/12 h (light/dark), the abundance of QH6 transcripts fluctuated in a diurnal pattern that ebbed around 3 h before daybreak (9th h in the dark phase) and peaked after 9 h in light (9th h in the light phase). The contents of (-)-beta-pinene in juvenile leaves and in emitted volatiles also varied in a diurnal rhythm, correlating strongly with mRNA accumulation. When A. annua was entrained by constant light or constant dark conditions, QH6 transcript accumulation continued to fluctuate with circadian rhythms. Under constant light, advanced cycles of fluctuation of QH6 transcript levels were observed, and under constant dark, the cycle was delayed. However, the original diurnal pattern could be regained when the plants were returned to the normal light/dark (12 h/12 h) photoperiod. This is the first report that monoterpene biosynthesis is transcriptionally regulated in a circadian pattern.
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A β-pinene synthase, which converts GPP to both (-)-α-pinene and (-)-β-pinene, has recently been described from A. annua.
“A β-pinene synthase, which converts GPP to both (-)-α-pinene (347) and (-)-β-pinene (356), has recently been described from A. annua [131].”
From The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao) (2010) · cites this paper as [131]
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Cites
Orchestrated Transcription of Key Pathways in <i>Arabidopsis</i> by the Circadian Clock
Harmer, S. L., Hogenesch, J. B., Straume, M., Chang, H.-S., Han, B., Zhu, T., Wang, X., Kreps, J. A., & Kay, S. A. (2000) · Science · doi:10.1126/science.290.5499.2110 · Cited by 1,640 · see citing works
Activation Tagging Identifies a Conserved MYB Regulator of Phenylpropanoid Biosynthesis
Borevitz, J., Xia, Y., Blount, J. W., Dixon, R. A., & Lamb, C. J. (2000) · The Plant Cell · doi:10.1105/tpc.12.12.2383 · Cited by 1,451 · see citing works
THE 1-DEOXY-D-XYLULOSE-5-PHOSPHATE PATHWAY OF ISOPRENOID BIOSYNTHESIS IN PLANTS
Lichtenthaler, H. K. (1999) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.50.1.47 · Cited by 1,403 · see citing works
Plant terpenoid synthases: Molecular biology and phylogenetic analysis
Bohlmann, J., Meyer-Gauen, G., & Croteau, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4126 · Cited by 1,122 · see citing works
Higher plant terpenoids: A phytocentric overview of their ecological roles
Langenheim, J. H. (1994) · Journal of Chemical Ecology · doi:10.1007/bf02059809 · Cited by 878 · see citing works
Biosynthesis and catabolism of monoterpenoids
Croteau, R. (1987) · Chemical Reviews · doi:10.1021/cr00081a004 · Cited by 599 · see citing works
Microarray Analysis of Diurnal and Circadian-Regulated Genes in Arabidopsis
Schaffer, R. J., Landgraf, J., Accerbi, M., Simon, V. A., Larson, M., & Wisman, E. (2001) · The Plant Cell · doi:10.1105/tpc.13.1.113 · Cited by 457 · see citing works
Mahmoud, S. S., & Croteau, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141237298 · Cited by 435 · see citing works
Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant.
Loughrin, J. H., Manukian, A., Heath, R. R., Turlings, T. C. J., & Tumlinson, J. H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11836 · Cited by 410 · see citing works
Biologically Active Substances from the GenusArtemisia
Tan, R. X., Zheng, W., & Tang, H. (1998) · Planta Medica · doi:10.1055/s-2006-957438 · Cited by 388 · see citing works
Regulation of Monoterpene Accumulation in Leaves of Peppermint
Gershenzon, J., McConkey, M. E., & Croteau, R. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.122.1.205 · Cited by 352 · see citing works
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 346 · see citing works
Plant Cytochrome P450 Monooxygenases
Schuler, M. A. (1996) · Critical Reviews in Plant Sciences · doi:10.1080/07352689609701942 · Cited by 335 · see citing works
A review and synthesis of monoterpene speciation from forests in the United States
Geron, C. D., Rasmussen, R. A., Arnts, R. R., et al. (2000) · Atmospheric Environment · doi:10.1016/s1352-2310(99)00364-7 · Cited by 322 · see citing works
Thompson, A. J., Jackson, A. C., Parker, R. A., Morpeth, D. R., Burbidge, A., & Taylor, I. B. (2000) · Plant Molecular Biology · doi:10.1023/a:1006448428401 · Cited by 286 · see citing works
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 · see citing works
Williams, D. C., McGarvey, D. J., Katahira, E. J., et al. (1998) · Biochemistry · doi:10.1021/bi980854k · Cited by 278 · see citing works
Amorpha-4,11-diene synthase catalyses the first probable step in artemisinin biosynthesis
Bouwmeester, H. J., Wallaart, T. E., Janssen, M. H. A., van Loo, B., Jansen, B. J. M., Posthumus, M. A., Schmidt, C. O., De Kraker, J.-W., König, W. A., & Franssen, M. C. R. (1999) · Phytochemistry · doi:10.1016/s0031-9422(99)00206-x · Cited by 266 · see citing works
Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants
Kolosova, N. P., Gorenstein, N., Kish, C. M., et al. (2001) · The Plant Cell · doi:10.1105/tpc.010162 · Cited by 248 · see citing works
Vogel, B. S., Wildung, M. R., Vogel, G., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.38.23262 · Cited by 247 · see citing works
Developmental Regulation of Monoterpene Biosynthesis in the Glandular Trichomes of Peppermint
McConkey, M. E., Gershenzon, J., & Croteau, R. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.122.1.215 · Cited by 246 · see citing works
Estévez, J. M., Cantero, A., Romero, C., Kawaide, H., Jiménez, L. F., Kuzuyama, T., Seto, H., Kamiya, Y., & León, P. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.124.1.95 · Cited by 240 · see citing works
Monoterpene Synthases from Grand Fir (Abies grandis)
Bohlmann, J., Steele, C. L., & Croteau, R. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.35.21784 · Cited by 219 · see citing works
Staudt, M., & Bertin, N. (1998) · Plant Cell & Environment · doi:10.1046/j.1365-3040.1998.00288.x · Cited by 211 · see citing works
Seasonal and diurnal patterns of monoterpene emissions from Pinus pinea (L.) under field conditions
Staudt, M., Bertin, N., Hansen, U., Seufert, G., Cicciolij, P., Foster, P., Frenzel, B., & Fugit, J. L. (1997) · Atmospheric Environment · doi:10.1016/s1352-2310(97)00081-2 · Cited by 185 · see citing works
Potrykus, I., & SPANGENBERG, G. C. (1995) · Springer eBooks · doi:10.1007/978-3-642-79247-2 · Cited by 154 · see citing works
Bertin, N., Staudt, M., Hansen, U., et al. (1997) · Atmospheric Environment · doi:10.1016/s1352-2310(97)00080-0 · Cited by 153 · see citing works
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 · see citing works
Isoprene synthesis by plants and animals
Sharkey, T. D. (1996) · Endeavour · doi:10.1016/0160-9327(96)10014-4 · Cited by 148 · see citing works
MONOTERPENE VARIATION IN PONDEROSA PINE XYLEM RESIN RELATED TO WESTERN PINE BEETLE PREDATION
Sturgeon, K. B. (1979) · Evolution · doi:10.1111/j.1558-5646.1979.tb04736.x · Cited by 145 · see citing works
Circadian rhythmicity in emission of volatile compounds by flowers of Rosa hybrida L. cv. Honesty
Helsper, J. P. F. G., Davies, J. A. R., Bouwmeester, H. J., et al. (1998) · Planta · doi:10.1007/s004250050459 · Cited by 131 · see citing works
Monoterpene and isoprene emissions from 15 Eucalyptus species in Australia
He, C., Murray, F., & Lyons, T. J. (2000) · Atmospheric Environment · doi:10.1016/s1352-2310(99)00219-8 · Cited by 130 · see citing works
Loreto, F., Ciccioli, P., Brancaleoni, E., et al. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9966 · Cited by 128 · see citing works
Emission of isoprene and carbonyl compounds from a boreal forest and wetland in Sweden
Janson, R. W., de Serves, C., & Romero, R. (1999) · Agricultural and Forest Meteorology · doi:10.1016/s0168-1923(99)00134-3 · Cited by 122 · see citing works
Regulation of Oleoresinosis in Grand Fir (Abies grandis)1
Steele, C. L., Katoh, S., Bohlmann, J., et al. (1998) · PLANT PHYSIOLOGY · doi:10.1104/pp.116.4.1497 · Cited by 120 · see citing works
Gambliel, H. A., & Croteau, R. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43520-4 · Cited by 111 · see citing works
Delfine, S., Csiky, O., Seufert, G., et al. (2000) · New Phytologist · doi:10.1046/j.1469-8137.2000.00612.x · Cited by 107 · see citing works
Mihaliak, C. A., Gershenzon, J., & Croteau, R. (1991) · Oecologia · doi:10.1007/bf00634594 · Cited by 103 · see citing works
Terpenoids from Artemisia annua and constituents of its essential oil
Ahmad, A., & Misra, L. N. (1994) · Phytochemistry · doi:10.1016/0031-9422(94)85021-6 · Cited by 87 · see citing works
Jia, J.-W., Crock, J., Lu, S., Croteau, R., & Chen, X.-Y. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1466 · Cited by 87 · see citing works
Self-citationBorg‐Karlson, A., Valterová, I., & Nilsson, L. A. (1993) · Phytochemistry · doi:10.1016/s0031-9422(00)90518-1 · Cited by 86 · see citing works
State of the art of the production of the antimalarial compound artemisinin in plants
Geldre, E. V., Vergauwe, A., & den Eeckhout, E. V. (1997) · Plant Molecular Biology · doi:10.1023/a:1005716600612 · Cited by 84 · see citing works
RAMPAGE: Promoter Activity Profiling by Paired-End Sequencing of 5′-Complete cDNAs
Batut, P. J., & Gingeras, T. (2013) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb25b11s104 · Cited by 79 · see citing works
Flora Novo-Galiciana: A Descriptive Account of the Vascular Plants of Western Mexico
Schmid, R., & Anderson, W. R. (1989) · Taxon · doi:10.2307/1222638 · Cited by 71 · see citing works
Signaling networks in the plant circadian system
Yanovsky, M. J., & Kay, S. A. (2001) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(00)00196-5 · Cited by 62 · see citing works
Light regulation of circadian clock‐controlled gene expression in rice
Sugiyama, N., Izawa, T., Oikawa, T., et al. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01063.x · Cited by 62 · see citing works
Standard Molecular Techniques for the Analysis of Transgenic Plants
Fütterer, J., Gisel, A., Iglesias, V., et al. (1995) · Springer eBooks · doi:10.1007/978-3-642-79247-2_25 · Cited by 61 · see citing works
Liu, C.-J., Heinstein, P. F., & Chen, X. (1999) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1999.12.12.1095 · Cited by 54 · see citing works
Self-citationBiogenic emissions and CO2 gas exchange investigated on four Mediterranean shrubs
Hansen, U., van Eijk, J., Bertin, N., et al. (1997) · Atmospheric Environment · doi:10.1016/s1352-2310(97)00082-4 · Cited by 52 · see citing works
Molecular scaffolds for chemical wizardry: Learning nature's rules for terpene cyclases
Greenhagen, B. T., & Chappell, J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261562898 · Cited by 44 · see citing works
Seasonal variations in monoterpene emissions from Eucalyptus species
He, C., Murray, F., & Lyons, T. J. (2000) · Chemosphere - Global Change Science · doi:10.1016/s1465-9972(99)00052-5 · Cited by 37 · see citing works
Bakrim, N., Brulfert, J., Vidal, J., et al. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5527 · Cited by 36 · see citing works
Picking out parallels: plant circadian clocks in context
McWatters, H. G., Roden, L. C., & Staiger, D. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0936 · Cited by 34 · see citing works
Structural studies in the bicyclo [3.1.1]heptane series by 1H and 13C NMR
Badjah‐Hadj‐Ahmed, A. Y., Meklati, B. Y., Waton, H., et al. (1992) · Magnetic Resonance in Chemistry · doi:10.1002/mrc.1260300902 · Cited by 30 · see citing works
Fluorescent Differential Display Identifies Circadian Clock-Regulated Genes in Arabidopsis thaliana
Kreps, J. A., Muramatsu, T., Furuya, M., et al. (2000) · Journal of Biological Rhythms · doi:10.1177/074873040001500302 · Cited by 23 · see citing works
A prenylated flavanone from Tephrosia maxima
Rao, E. V., Prasad, Y. R., & Murthy, M. S. R. (1994) · Phytochemistry · doi:10.1016/0031-9422(94)85007-0 · Cited by 20 · see citing works
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Research works printed but not linked: 2
- Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current Protocols in Molecular Biology. New York: John Wiley & Sons; 1995. [Google Scholar]
- Croteau R. Biosynthesis and metabolism of monoterpenes. Chem Rev. 1987;87:929–954. [Google Scholar]
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The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao)
Brown, G. D. (2010) · Molecules · doi:10.3390/molecules15117603 · Cited by 363 · see citing works
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Markus Lange, B., & Turner, G. W. (2013) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2012.00737.x · Cited by 195 · see citing works
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 · see citing works
Weathers, P. J., Elkholy, S., & Wobbe, K. K. (2006) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1079/ivp2006782 · Cited by 97 · see citing works
- Authors
- Lu, S., Xu, R., Jia, J.-W., Pang, J., Matsuda, S. P. T., & Chen, X.-Y.
- Affiliations
- Chinese Academy of Sciences (CN)
- Rice University (US)
- National Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (S.L., J.-W.J., X.-Y.C.); and Departments of
- Venue
- PLANT PHYSIOLOGY
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-09-01
- Volume
- 130
- Issue
- 1
- Pages
- 477-486
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC166579
- OpenAlex
- W2088897516
- Cited by
- 108
- References
- 56
- Citations by year
- 2026: 1 · 2025: 8 · 2024: 7 · 2023: 2 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 4 · 2015: 5 · 2014: 8 · 2013: 5 · 2012: 3
- FWCI
- 0.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- PLANT PHYSIOLOGY (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ai041598-04)
- National Institute of Allergy and Infectious Diseases (AI 41598)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
- Keywords
- Artemisia annua, monoterpene biosynthesis, circadian rhythm, diurnal gene expression, geranyl diphosphate, volatile compounds, plant defense response, photoperiod entrainment, transcriptional regulation
- MeSH terms
- Bicyclic Monoterpenes, Amino Acid Sequence, Base Sequence, Bridged Bicyclo Compounds, Circadian Rhythm, Cloning, Molecular, Light, Molecular Sequence Data, Phylogeny, Plant Proteins, Transcription Factors, Gene Expression Regulation, Enzymologic, Sequence Analysis, DNA, DNA, Complementary, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Plant Stems, Intramolecular Lyases, Artemisia annua, Monoterpenes
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