A Genome-Wide Scenario of Terpene Pathways in Self-pollinated Artemisia annua

Ma, Dong-Ming; Wang, Zhilong; Wang, Liangjiang; Alejos-Gonzales, Fatima; Sun, Ming-An; Xie, De-Yu

doi:10.1016/j.molp.2015.07.004

Cited by 83Plant biochemistry and biosynthesisPlant tissue culture and regenerationSesquiterpenes and Asteraceae Studies

A Genome-Wide Scenario of Terpene Pathways in Self-pollinated Artemisia annua

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Ma, Dong-Ming, Wang, Zhilong, Wang, Liangjiang, Alejos-Gonzales, Fatima, Sun, Ming-An, Xie, De-Yu·2015·Molecular Plant

DOI 10.1016/j.molp.2015.07.004

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Abstract

Scenarios of genes to metabolites in Artemisia annua remain uninvestigated. Here, we report the use of an integrated approach combining metabolomics, transcriptomics, and gene function analyses to characterize gene-to-terpene and terpene pathway scenarios in a self-pollinating variety of this species. Eighty-eight metabolites including 22 sesquiterpenes (e.g., artemisinin), 26 monoterpenes, two triterpenes, one diterpene and 38 other non-polar metabolites were identified from 14 tissues. These metabolites were differentially produced by leaves and flowers at lower to higher positions. Sequences from cDNA libraries of six tissues were assembled into 18 871 contigs and genome-wide gene expression profiles in tissues were strongly associated with developmental stages and spatial specificities. Sequence mining identified 47 genes that mapped to the artemisinin, non-amorphadiene sesquiterpene, monoterpene, triterpene, 2-C-methyl-D-erythritol 4-phosphate and mevalonate pathways. Pearson correlation analysis resulted in network integration that characterized significant correlations of gene-to-gene expression patterns and gene expression-to-metabolite levels in six tissues simultaneously. More importantly, manipulations of amorpha-4,11-diene synthase gene expression not only affected the activity of this pathway toward artemisinin, artemisinic acid, and arteannuin b but also altered non-amorphadiene sesquiterpene and genome-wide volatile profiles. Such gene-to-terpene landscapes associated with different tissues are fundamental to the metabolic engineering of artemisinin.

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Recent attempts to knock down the amorpha-4,11-diene synthase using RNAi in self-pollinating A. annua resulted in only a modest (30-50%) reduction in artemisinin levels.
“Recent attempts to knock down the amorpha-4,11-diene synthase using RNAi in self-pollinating A. annua resulted in only a modest (30-50%) reduction in artemisinin levels (25).”
From Artemisia annua mutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism (2016) · cites this paper as [25]

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Artemisia annua mutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism
Czechowski, T., Larson, T. R., Catania, T. M., Harvey, D., Brown, G. D., & Graham, I. A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611567113 · Cited by 94 · see citing works
Artemisinin Biosynthesis in Non-glandular Trichome Cells of Artemisia annua
Judd, R., Bagley, M. C., Li, M., Zhu, Y., Lei, C., Yuzuak, S., Ekelöf, M., Pu, G., Zhao, X., Muddiman, D. C., et al. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.02.011 · Cited by 75 · see citing works
Self-citation
Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches
Wani, K. I., Choudhary, S., Zehra, A., Naeem, M., Weathers, P., & Aftab, T. (2021) · Planta · doi:10.1007/s00425-021-03676-3 · Cited by 74 · see citing works
Artemisinin biosynthesis in Artemisia annua and metabolic engineering: questions, challenges, and perspectives
Xie, D.-Y., Ma, D.-M., Judd, R., & Jones, A. L. (2016) · Phytochemistry Reviews · doi:10.1007/s11101-016-9480-2 · Cited by 63 · see citing works
Self-citation

Is Artemisinin the Only Antiplasmodial Compound in the Artemisia annua Tea Infusion? An in Vitro Study
Mouton, J., Jansen, O., Frédérich, M., & van der Kooy, F. (2013) · Planta Medica · doi:10.1055/s-0032-1328324 · Cited by 20 · see citing works
Artemisia annua glandular secretory trichomes： the biofactory of antimalarial agent artemisinin
Ling, Xiao, X., Hexin, et al. (2016) · 中国科学通报：英文版
A review of various efforts to increase artemisinin and other antimalarial compounds in Artemisia Annua L plant
Aidah, N., Bazira, J., Tolo, C. U., & Engeu, P. O. (2018) · Cogent Biology · doi:10.1080/23312025.2018.1513312 · Cited by 16 · see citing works
Self-immobilized aggreage culture of Artemisia annua L. for imroved artemisinin
Hu, F., Chen, C.-L., & Guanlin, W. (2003) · Zhiwu yanjiu
Metabolic engineering of artemisinin biosynthesis in Artemisia annua L.
Liu, B., Wang, H., Du, Z., Li, G., & Ye, H. (2010) · Plant Cell Reports · doi:10.1007/s00299-010-0967-9 · Cited by 82 · see citing works

Authors: Ma, D.-M., Wang, Z., Wang, L., Alejos-Gonzales, F., Sun, M.-A., & Xie, D.-Y.
Affiliations: North Carolina State University (US)
Clemson University (US)
Virginia Tech (US)
Corresponding author: Xie, De-Yu
ORCID: Wang, Zhilong
Wang, Liangjiang
Sun, Ming-An
Xie, De-Yu
Venue: Molecular Plant
Publisher: Elsevier BV
Published: 2015-11
Volume: 8
Issue: 11
Pages: 1580-1598
ISSN: 1674-2052 (ISSN-L)
DOI: 10.1016/j.molp.2015.07.004
OpenAlex: W1913281859
Cited by: 83
References: 81
Citations by year: 2026: 5 · 2025: 2 · 2024: 5 · 2023: 11 · 2022: 8 · 2021: 18 · 2020: 3 · 2019: 10 · 2018: 8 · 2017: 7 · 2016: 5 · 2015: 1
FWCI: 3.04
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 367 d)
Locations: Molecular Plant (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Sesquiterpenes and Asteraceae Studies
Keywords: Artemisia annua, terpene biosynthesis, artemisinin biosynthesis, sesquiterpenes, monoterpenes, triterpenoids, amorpha-4,11-diene synthase, gene regulatory networks, 2-C-methyl-D-erythritol 4-phosphate pathway, mevalonate pathway, tissue-specific metabolism, volatile compounds, metabolic engineering
MeSH terms: Gas Chromatography-Mass Spectrometry, Terpenes, Genes, Plant, Gene Expression Profiling, Artemisia annua, Artemisinins, Pollination, Metabolomics, Self-Fertilization

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A Genome-Wide Scenario of Terpene Pathways in Self-pollinated Artemisia annua

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