Abstract
BackgroundOpium poppy (Papaver somniferum) produces a diverse array of bioactive benzylisoquinoline alkaloids and has emerged as a model system to study plant alkaloid metabolism. The plant is cultivated as the only commercial source of the narcotic analgesics morphine and codeine, but also produces many other alkaloids including the antimicrobial agent sanguinarine. Modulations in plant secondary metabolism as a result of environmental perturbations are often associated with the altered regulation of other metabolic pathways. As a key component of our functional genomics platform for opium poppy we have used proton nuclear magnetic resonance (1H NMR) metabolomics to investigate the interplay between primary and secondary metabolism in cultured opium poppy cells treated with a fungal elicitor.ResultsMetabolite fingerprinting and compound-specific profiling showed the extensive reprogramming of primary metabolic pathways in association with the induction of alkaloid biosynthesis in response to elicitor treatment. Using Chenomx NMR Suite v. 4.6, a software package capable of identifying and quantifying individual compounds based on their respective signature spectra, the levels of 42 diverse metabolites were monitored over a 100-hour time course in control and elicitor-treated opium poppy cell cultures. Overall, detectable and dynamic changes in the metabolome of elicitor-treated cells, especially in cellular pools of carbohydrates, organic acids and non-protein amino acids were detected within 5 hours after elicitor treatment. The metabolome of control cultures also showed substantial modulations 80 hours after the start of the time course, particularly in the levels of amino acids and phospholipid pathway intermediates. Specific flux modulations were detected throughout primary metabolism, including glycolysis, the tricarboxylic acid cycle, nitrogen assimilation, phospholipid/fatty acid synthesis and the shikimate pathway, all of which generate secondary metabolic precursors.ConclusionThe response of cell cultures to elicitor treatment involves the extensive reprogramming of primary and secondary metabolism, and associated cofactor biosynthetic pathways. A high-resolution map of the extensive reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures is provided.
Highlights
Opium poppy (Papaver somniferum) produces a diverse array of bioactive benzylisoquinoline alkaloids and has emerged as a model system to study plant alkaloid metabolism
Metabolite profiling by 1H nuclear magnetic resonance (NMR) is a useful tool to characterize the metabolic response of plant cell cultures to environmental perturbations, such as elicitor treatment [8,9]
The identification of additional metabolites will require the fractionation of cellular extracts to reduce masking by abundant metabolites, and the addition of reference compounds to the signature spectra database
Summary
Opium poppy (Papaver somniferum) produces a diverse array of bioactive benzylisoquinoline alkaloids and has emerged as a model system to study plant alkaloid metabolism. Opium poppy (Papaver somniferum) is the world's oldest medicinal plant and produces several pharmaceutically important benzylisoquinoline alkaloids, including the analgesics morphine and codeine, the muscle relaxant and vasodilator papaverine, the antineoplastic drug noscapine and the antimicrobial agent sanguinarine. Opium poppy cell cultures do not constitutively accumulate alkaloids, and produce only sanguinarine in response to treatment with specific fungal elicitors [7]. Elicitor-induced sanguinarine biosynthesis in opium poppy cell cultures provides a platform to definitively characterize the environmental induction of alkaloid and other secondary metabolic pathways under precisely controlled conditions. The establishment of an extensive array of genomics resources, including expressed sequence tags (ESTs) and DNA microarrays [8], for opium poppy plants and cell cultures has accelerated the development of a systems biology approach to discover new alkaloid biosynthetic genes and relevant biological processes
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