Control of resource allocation between primary and specialized metabolism in glandular trichomes

Brand, Alejandro; Tissier, Alain

doi:10.1016/j.pbi.2022.102172

Cited by 6 publications

(6 citation statements)

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“…Transcription factors that drive high expression of enzymes involved in both primary and secondary metabolism in GTs have been identified. Many of these, however, also have effects on trichome development making separating their direct roles in enzyme expression from indirect developmental effects challenging (Brand & Tissier, 2022). Gene duplication also appears to be important as it permits the evolution of enzyme isoforms associated with the specialized metabolism of GT cells (Brand & Tissier, 2022).…”

Section: Glandular Trichomesmentioning

confidence: 99%

“…Many of these, however, also have effects on trichome development making separating their direct roles in enzyme expression from indirect developmental effects challenging (Brand & Tissier, 2022). Gene duplication also appears to be important as it permits the evolution of enzyme isoforms associated with the specialized metabolism of GT cells (Brand & Tissier, 2022). For example, type II isoforms of DXS, the first enzyme of the MEP pathway, tend to be associated with isoprene-producing tissues.…”

Section: Glandular Trichomesmentioning

confidence: 99%

“…Indeed, tobacco GTs express a specific form of the ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RubisCO) small subunit that has a relatively high turnover but low CO 2 affinity, and which may therefore be suited to the high‐CO 2 concentration conditions of GTs (Laterre et al., 2017). Further study is required though as this small subunit isoform is not present in some species where refixation of CO 2 released by respiration is known to occur, such as B. napus (Brand & Tissier, 2022). Interestingly, epithelial duct cells isolated from loblolly pine ( Pinus taeda ) needles using LAM that produce diterpenes, sesquiterpenes and monoterpenes as part of their oleoresin appear to have a similar metabolism to cells of GTs of herbaceous species, showing high MEP pathway activity, ATP synthesis, heterotrophic regeneration of ferredoxin and fermentation (Turner et al., 2019).…”

Section: Cell‐type‐specific Metabolic Phenotypesmentioning

confidence: 99%

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Cell‐type‐specific metabolism in plants

et al. 2023

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SUMMARY Every plant organ contains tens of different cell types, each with a specialized function. These functions are intrinsically associated with specific metabolic flux distributions that permit the synthesis of the ATP, reducing equivalents and biosynthetic precursors demanded by the cell. Investigating such cell‐type‐specific metabolism is complicated by the mosaic of different cells within each tissue combined with the relative scarcity of certain types. However, techniques for the isolation of specific cells, their analysis in situ by microscopy, or modeling of their function in silico have permitted insight into cell‐type‐specific metabolism. In this review we present some of the methods used in the analysis of cell‐type‐specific metabolism before describing what we know about metabolism in several cell types that have been studied in depth; (i) leaf source and sink cells; (ii) glandular trichomes that are capable of rapid synthesis of specialized metabolites; (iii) guard cells that must accumulate large quantities of the osmolytes needed for stomatal opening; (iv) cells of seeds involved in storage of reserves; and (v) the mesophyll and bundle sheath cells of C4 plants that participate in a CO2 concentrating cycle. Metabolism is discussed in terms of its principal features, connection to cell function and what factors affect the flux distribution. Demand for precursors and energy, availability of substrates and suppression of deleterious processes are identified as key factors in shaping cell‐type‐specific metabolism.

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Section: Glandular Trichomesmentioning

confidence: 99%

Section: Glandular Trichomesmentioning

confidence: 99%

Section: Cell‐type‐specific Metabolic Phenotypesmentioning

confidence: 99%

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Cell‐type‐specific metabolism in plants

et al. 2023

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“…Even research focused on light intensity‐mediated trichome production does not focus on their photosynthetic activity (Escobar‐Bravo et al., 2018). The separation of cytosolic and chloroplast‐bound pathways, as well as the utility of photosynthesis, are until now only vaguely understood, and the most recent summary of current advances has been recently provided (Brand & Tissier, 2022).…”

Section: Introductionmentioning

confidence: 99%

Shifts in carbon partitioning by photosynthetic activity increase terpenoid synthesis in glandular trichomes

et al. 2023

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SUMMARYSeveral 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.

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“…It is still unclear what the advantages and disadvantages of photosynthetic GTs, are in contrast to non-photosynthetic GTs. The separation of cytosolic and chloroplast bound pathways, as well as the utility of photosynthesis, are until now only vaguely understood, and the most recent summary of current advances has been recently provided [5].…”

Section: Introductionmentioning

confidence: 99%

Shifts in carbon partitioning by photosynthetic activity increase terpenoid synthesis in glandular trichomes

Saadat

Aalst

Ebenhöh

et al. 2022

Preprint

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Several commercially important secondary metabolites are produced and accumulated in high amounts by glandular trichomes (GTs), giving the prospect of exploiting trichomes as metabolic cell factories. Due to extremely high metabolic fluxes through GT particular attention was drawn to how they are achieved. The question regarding bioenergetics of these dedicated structures becomes more interesting when one realizes that some cells are photosynthetically active. Despite recent advances, how primary metabolism contributes to GTs high metabolic fluxes is still not fully elucidated. We provide the first reconstruction of specialised metabolism in photosynthetic glandular trichomes of Solanum lycopersicum. With increasing light intensities our model shows a shift of carbon partitioning from catabolic to anabolic reactions driven by the energy availability of the cell. Moreover, we show the benefit of using MEV or MEP pathways under different light conditions. Lastly, we can observe the refixation of the CO2 by RuBisCO in high light conditions. The outcomes of this research close an important gap in knowledge of the role of chloroplast in the synthesis of specialised metabolites in plants' GTs.

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Control of resource allocation between primary and specialized metabolism in glandular trichomes

Cited by 6 publications

References 70 publications

Cell‐type‐specific metabolism in plants

Cell‐type‐specific metabolism in plants

Shifts in carbon partitioning by photosynthetic activity increase terpenoid synthesis in glandular trichomes

Shifts in carbon partitioning by photosynthetic activity increase terpenoid synthesis in glandular trichomes

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