Modelling Processes Determining and Limiting the Production of Secondary Metabolites During Crop Growth: The Example of the Antimalarial Artemisinin Produced in Artemisia Annua

Abstract

The quantitative insight in processes underlying yield and concentrations of interesting secondary metabolites in crops is still limited. Yet, this insight is essential to further improve crops and commercial production of target metabolites. Artemisia annua L. (annual or sweet wormwood, Asteraceae) was used to conceptualize a model to describe the processes determining and limiting the production of target metabolites during crop growth. A. annua is an annual herb producing the antimalarial artemisinin, a sesquiterpene lactone with an endoperoxide bridge. Artemisinin is predominantly produced in glandular trichomes present on the leaves and inflorescences. Leaves are the most important organs harvested in commercial production. The accumulation of artemisinin in the crop was analysed as the resultant of the key processes determining leaf dry weight production, accumulation of artemisinin in the leaves and losses after synthesis. A yield formation modelling approach was used to quantify artemisinin yield as a function of the individual processes and to study which processes limited production. Leaf dry weight production was limited by low total dry matter production of the crop because of poor radiation interception during early canopy expansion, and by a high proportion of dry matter allocated to stems that do not contribute to artemisinin production. Production of the target metabolite in the leaves was limited because the total production of artemisinin precursors per unit leaf dry weight was low and because the conversion of precursors to artemisinin was only partial. Possibilities to increase the values of the different yield components are discussed. A new, simple, model for explaining variation in artemisinin yield based on leaf and trichome production in combination with biosynthesis of artemisinin is proposed. INTRODUCTIONInterest in plant secondary metabolites that have a protective or curative effect on human diseases has been renewed. These compounds can be taken in as drugs or as part of food and beverages. Yields and concentrations of target metabolites in crops or crop products are usually low and highly variable over studies. Also within crops, concentrations vary. The causes of these fluctuations are often unknown because commercial production methods are commonly based on applied dose-effect studies with limited attention to the crop physiology behind the effects. A great need exists for more insight into the different processes underlying the accumulation of the secondary metabolites of interest. An improved understanding can lead to more stable yield levels and concentrations, better breeding strategies, more founded selection of production environments, and agronomical and technological innovations in the production chain.To achieve a full and quantitative understanding of accumulation of secondary metabolites is difficult because mechanisms underlying their yields and concentrations in crops are more complex than those underlying yield of plant organs, yield of primary

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“…A combination of factors may be important. Such is the case for Artemisia annua , where yield of the antimalarial compound artemisinin depends on leaf dry weight, availability of metabolic precursors, and efficiency of conversion to end products, in addition to trichome density (Lommen et al, 2008).…”

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“…Medicinal and aromatic plants (MAPs) changed their chemical profile in different ecological conditions in order to adapt to the environment. [1] [2] Therefore, the populations of a medicinal species that are growing in various natural habitats show the variability in the quantity and quality of active ingredients, which lead to differences in their pharmacological and biological activity. [3 -5] The genetic flexibility of plant populations makes this variation possible and then gradually leads to arise some individuals which are different in chemical and botanical characteristics.…”

“…Medicinal and aromatic plants (MAPs) changed their chemical profile in different ecological conditions in order to adapt to the environment . Therefore, the populations of a medicinal species that are growing in various natural habitats show the variability in the quantity and quality of active ingredients, which lead to differences in their pharmacological and biological activity .…”