Institute of Theoretical and Quantitative Biology, Heinrich Heine University Düsseldorf, 40225, Düsseldorf, Germany.
Cluster of Excellence on Plant Sciences, Heinrich Heine University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.
Plant J. 2023 Sep;115(6):1716-1728. doi: 10.1111/tpj.16352. Epub 2023 Jul 4.
Several commercially important secondary metabolites are produced and accumulated in high amounts by glandular trichomes, giving the prospect of using them as metabolic cell factories. Due to extremely high metabolic fluxes through glandular trichomes, previous research focused on how such flows are achieved. The question regarding their bioenergetics became even more interesting with the discovery of photosynthetic activity in some glandular trichomes. Despite recent advances, how primary metabolism contributes to the high metabolic fluxes in glandular trichomes is still not fully elucidated. Using computational methods and available multi-omics data, we first developed a quantitative framework to investigate the possible role of photosynthetic energy supply in terpenoid production and next tested experimentally the simulation-driven hypothesis. With this work, we provide the first reconstruction of specialised metabolism in Type-VI photosynthetic glandular trichomes of Solanum lycopersicum. Our model predicted that increasing light intensities results in a shift of carbon partitioning from catabolic to anabolic reactions driven by the energy availability of the cell. Moreover, we show the benefit of shifting between isoprenoid pathways under different light regimes, leading to a production of different classes of terpenes. Our computational predictions were confirmed in vivo, demonstrating a significant increase in production of monoterpenoids while the sesquiterpenes remained unchanged under higher light intensities. The outcomes of this research provide quantitative measures to assess the beneficial role of chloroplast in glandular trichomes for enhanced production of secondary metabolites and can guide the design of new experiments that aim at modulating terpenoid production.
几种具有商业重要性的次生代谢物由腺毛大量产生和积累，为将其用作代谢细胞工厂提供了前景。由于腺毛中存在极高的代谢通量，先前的研究主要集中在如何实现这些通量。随着发现一些腺毛具有光合作用活性，关于它们的生物能量学的问题变得更加有趣。尽管最近取得了进展，但初级代谢物如何为腺毛中的高代谢通量做出贡献仍未完全阐明。我们首先使用计算方法和现有的多组学数据，开发了一个定量框架来研究光合作用能量供应在萜类化合物生产中的可能作用，然后通过实验测试了模拟驱动的假设。通过这项工作，我们提供了番茄（Solanum lycopersicum）VI 型光合腺毛特化代谢物的首次重建。我们的模型预测，增加光强会导致细胞能量可用性驱动的碳分配从分解代谢向合成代谢转移。此外，我们展示了在不同光照条件下在异戊二烯途径之间切换的好处，从而产生不同类别的萜类化合物。我们的计算预测在体内得到了证实，证明在高光强下，单萜类化合物的产量显著增加，而倍半萜类化合物保持不变。这项研究的结果提供了定量措施来评估叶绿体在腺毛中对次生代谢物增强生产的有益作用，并可以指导旨在调节萜类化合物生产的新实验的设计。
