Biologia plantarum 55:669, 2011 | DOI: 10.1007/s10535-011-0166-8

Singlet oxygen as a signaling transducer for modulating artemisinin biosynthetic genes in Artemisia annua

Q. -P. Zeng1,*, X. -M. Zeng1, R. -Y. Yang1, X. -Q. Yang1
1 Laboratory of Biotechnology, Tropical Medicine Institute, Guangzhou University of Chinese Medicine, Guangzhou, P.R. China

Although crosstalk between cytosolic and plastidic terpenoid pathways has been validated in many plant species, we report here for the first time a striking elevation of the nucleus-encoded artemisinin biosynthesis relevant DBR2 mRNA following the incubation of plants with fosmidomycin (FM). FM decreased singlet oxygen (1O2) scavengers such as β-carotene and α-tocopherol and subsequently invoked 1O2 burst. The treatment of plants with fluridone (FD) neither decreased α-tocopherol content nor triggered 1O2 emission. In conclusion, FM can up-regulate 1O2-sensitive nuclear genes responsible for artemisinin biogenesis by mitigating the accumulation of plastidic scavenging terpenoids, thereby eliciting 1O2 generation and initiating 1O2 retrograde signaling.

Keywords: fosmidomycin; fluridone; gene expression; reactive oxygen species; upregulation

Received: December 18, 2009; Accepted: November 12, 2010; Published: December 1, 2011Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Zeng, Q.-P., Zeng, X.-M., Yang, R.-Y., & Yang, X.-Q. (2011). Singlet oxygen as a signaling transducer for modulating artemisinin biosynthetic genes in Artemisia annua. Biologia plantarum, 55(4), 669. doi: 10.1007/s10535-011-0166-8.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Bartels, P.G., Watson, C.W.: Inhibition of carotenoid synthesis by fluridone and norflurazon. - Weed Sci. 26: 198-203, 1978. Go to original source...
    2. Benderliev, K.M., Ivanova, N.I., Pilarski, P.S.: Singlet oxygen and other reactive oxygen species are involved in regulation of release of iron-binding chelators from Scenedesmus cells. - Biol. Plant. 47: 523-526, 2003.
    3. 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., Franssen, M.C., Bouwmeester, H.J.: Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. - Planta med. 71: 40-47, 2005. Go to original source...
    4. Bertea, C.M., Voster, A., Verstappen, F.W., Maffei, M., Beekwilder, J., Bouwmeester, H.J.: Isoprenoid biosynthesis in Artemisia annua: cloning and heterologous expression of a germacrene A synthase from a glandular trichome cDNA library. - Arch. Biochem. Biophys. 448: 3-12, 2006. Go to original source...
    5. Chappell, J.: The genetics and molecular genetics of terpene and sterol origami. - Curr. Opin. Plant Biol. 5: 151-157, 2002. Go to original source...
    6. Covello, P. S.: Making artemisinin. - Phytochemistry 69: 2881-2885, 2008. Go to original source...
    7. Covello, P.S., Teoh, K.H., Polichuk, D.R., Reed, D.W., Nowak, G.: Functional genomics and the biosynthesis of artemisinin. - Phytochemistry 68: 1864-1871, 2007.
    8. Feng, L.L., Yang, R.Y., Yang, X.Q., Zeng, X.M., Lu, W.J., Zeng, Q.P.: Synergistic re-channeling of mevalonate pathway for artemisinin overproduction in transgenic Artemisia annua. - Plant Sci. 177: 57-67, 2009. Go to original source...
    9. Guo, X.X., Yang, X.Q., Yang, R.Y., Zeng, Q.P.: Salicylic acid and methyl jasmonate but not Rose Bengal up-regulate artemisinin biosynthetic genes through invoking burst of endogenous singlet oxygen. - Plant Sci. 178: 390-397, 2010. Go to original source...
    10. Hirayama, O., Nakamura, K., Hamada, S., Kobayashi, Y.: Singlet oxygen quenching ability of naturally occurring carotenoids. - Lipids 29: 149-150, 1994. Go to original source...
    11. Kim, S.H., Chang, Y.J., Kim, S.U.: Tissue specificity and developmental pattern of amorpha-4,11-diene synthase (ADS) proved by ADS promoter-driven GUS expression in the heterologous plant, Arabidopsis thaliana. - Planta med. 74: 188-193, 2008. Go to original source...
    12. Laloi, C., Przybyla, D., Apel, K.: A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana.- J. exp. Bot. 57: 1719-1724, 2006. Go to original source...
    13. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, I.M., Apel, K.: Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signalling of stress responses in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 104: 672-677, 2007. Go to original source...
    14. Laule, O., Furholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., Lange, M.: Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 100: 6866-6871, 2003. Go to original source...
    15. Lee, K.P., Kim, C., Landgraf, F., Apel, K.: EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. -Proc. nat. Acad. Sci. USA 104: 10270-10275, 2007. Go to original source...
    16. Maeda, H., Sakuragi, Y., Bryant, D.A., Della Penna, D.: Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. - Plant Physiol. 138: 1422-1435, 2005. Go to original source...
    17. Ro, D.K., Paradise, E.M., Ouelle, t M., Fisher, K.J., Newman, K.L., Ndungu, J.M., Ho, K.A., Eachus, R.A., Ham, T.S., Kirby, J., Chang, M.C., Withers, S.T., Shiba, Y., Sarpong, R., Keasling, J.D.: Production of the antimalarial drug precursor artemisinic acid in engineered yeast. - Nature 440: 940-943, 2006. Go to original source...
    18. Rodriguez-Concepcion, M., Fores, O., Martinez-Garcia, J.F., Gonzalez, V., Phillips, M.A., Ferrer, A., Boronat, A.: Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. - Plant Cell 16: 144-156, 2004. Go to original source...
    19. Sy, L.K., Brown, G.D.: The mechanism of the spontaneous autoxidation of dihydroartemisinic acid. - Tetrahedron 58: 897-908, 2002. Go to original source...
    20. Teoh, K.H., Polichuk, D.R., Reed, D.W., Nowak, G., Covello, P. S.: 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, 2006. Go to original source...
    21. Towler, M.J., Weathers, P.J.: Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. - Plant Cell Rep. 26: 2129-2136, 2007. Go to original source...
    22. Triantaphylides, C., Havaux, M.: Singlet oxygen in plants: production, detoxification and signaling. - Trends Plant Sci. 14: 219-228, 2009. Go to original source...
    23. Wallaart, T.E., Van Uden, W., Lubberink, H.G.M., Woerdenbag, H.J., Pras, N., Quax, W.J.: Isolation and identification of dihydroartemisinic acid from Artemisia annua and its possible role in the biosynthesis of artemisinin. - J. natur. Prod. 62: 430-433, 1999. Go to original source...
    24. Wu, S., Schalk, M., Clark, A., Miles, R.B., Coates, R., Chappell, J.: Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. - Nat. Biotechnol. 24: 1441-1447, 2006. Go to original source...
    25. Xu, X., Hu, X., Neill, S.J., Fang, J., Cai, W.: Fungal elicitor induces singlet oxygen generation, ethylene release and saponin synthesis in cultured cells of Panax ginseng C.A. Meyer. - Plant Cell Physiol. 46: 947-954, 2005. Go to original source...
    26. Yang, R.Y., Feng, L.L., Yang, X.Q., Yin, L.L., Xu, X.L., Zeng, Q.P.: Quantitative transcript profiling reveals downregulation of a steroid pathway relevant gene and overexpression of artemisinin biogenetic genes in transgenic Artemisia annua plants. - Planta med. 74: 1510-1516, 2008. Go to original source...
    27. Yang, R.Y., Zeng, X.M., Lu, Y.Y., Lu, W.J., Feng, L.L., Yang, X.Q., Zeng, Q.P.: Senescent leaves of Artemisia annua are one of the most active organs for overexpression of artemisinin biosynthesis responsible genes upon burst of singlet oxygen. - Planta med. 76: 734-742, 2010. Go to original source...
    28. Yin, L.L., Zhao, C., Huang, Y., Yang, R.Y.: Abiotic stressinduced expression of artemisinin biosynthesis genes in Artemisia annua L. - Chin. appl. environ. Biol. 14: 1-5, 2008.
    29. Zeng, Q.P., Qiu, F., Yuan, L.: Production of artemisinin by genetically modified microbes. - Biotechnol. Lett. 30: 581-592, 2008a. Go to original source...
    30. Zeng, Q.P., Yang, R.Y., Feng, L.L., Yang, X.Q.: Genetic and environmental regulation and artificial metabolic manipulation for artemisinin biosynthesis. - In: Richter, F.W. (ed.): Biotechnology: Research, Technology and Applications. Pp. 159-210. Nova Science Publishers, New York 2008b.
    31. Zeng, Q.P., Zeng, X.M., Feng, L.L., Yin, L.L., Yang, X.Q., Yang, R.Y.: Quantification of three key enzymes involved in artemisinin biosynthesis in Artemisia annua by polyclonal antisera-based ELISA. - Plant mol. Biol. Rep. 27: 50-57, 2009. Go to original source...
    32. Zeng, Q.P., Zhao, C., Yin, L.L., Yang, R.Y., Zeng, X.M., Huang, Y., Feng, L.L., Yang, X.Q.: Cloning of artemisinin biosynthetic cDNAs and novel ESTs and quantification of low temperature-induced gene overexpression. - Sci. China Ser. C 51: 232-244, 2008c. Go to original source...
    33. Zhang, Y.S., Teoh, K.H., Reed, D.W., Maes, L., Goossens, A., Olson, D.J.H., Ross, A.R.S., Covello, P.S.: The molecular cloning of artemisinic aldehyde Δ11 (13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. - J. biol. Chem. 283: 21501-21508, 2008. Go to original source...

    Return to the content