Bioenergetics of Monoterpenoid Essential Oil Biosynthesis in Nonphotosynthetic Glandular Trichomes

Abstract

ORCID IDs: 0000-0001-8261-9015 (S.R.J.); 0000-0001-7934-7987 (N.S.); 0000-0001-6565-9584 (B.M.L.).The commercially important essential oils of peppermint (Mentha 3 piperita) and its relatives in the mint family (Lamiaceae) are accumulated in specialized anatomical structures called glandular trichomes (GTs). A genome-scale stoichiometric model of secretory phase metabolism in peppermint GTs was constructed based on current biochemical and physiological knowledge. Fluxes through the network were predicted based on metabolomic and transcriptomic data. Using simulated reaction deletions, this model predicted that two processes, the regeneration of ATP and ferredoxin (in its reduced form), exert substantial control over flux toward monoterpenes. Follow-up biochemical assays with isolated GTs indicated that oxidative phosphorylation and ethanolic fermentation were active and that cooperation to provide ATP depended on the concentration of the carbon source. We also report that GTs with high flux toward monoterpenes express, at very high levels, genes coding for a unique pair of ferredoxin and ferredoxin-NADP + reductase isoforms. This study provides, to our knowledge, the first evidence of how bioenergetic processes determine flux through monoterpene biosynthesis in GTs.

Assessment of flux through oleoresin biosynthesis in epithelial cells of loblolly pine resin ducts

“…The insufficient sequencing depth of our transcriptome data and the paucity of literature reporting on conifer ferredoxin and FNR prevented us from assessing whether epithelial cells of loblolly pine resin ducts may contain a similar arrangement of isoforms. We also demonstrated previously that both oxidative phosphorylation and fermentation were highly active to recycle energy equivalents in non-photosynthetic peppermint glandular trichomes (Johnson et al , 2017). Genes involved in both processes were found to be enriched in the loblolly pine epithelial cell transcriptome (compared with mesophyll cells) (Supplementary Table S4).…”

“…4B). Detailed considerations for developing objective functions for secretory cell types are provided in Johnson et al (2017). The incorporation of metabolically synthesized amino acids into total protein was calculated based on the amino acid composition of glutathione S -transferase, the enzyme encoded by the most highly expressed non-photosynthetic gene of this cell type.…”

“…A particularly high flux was predicted to occur through the MEP pathway of epithelial cells, where two reactions—those catalyzed by the iron-sulfur cluster enzymes 1-hydroxy-2-methyl-2-( E )-butenyl-4-diphosphate synthase and 1-hydroxy-2-methyl-2-( E )-butenyl-4-diphosphate reductase—require electron transfer through the ferredoxin/FNR system. We recently demonstrated the presence of a unique pair of ferredoxin and FNR isoforms in secretory cells of peppermint glandular trichomes (Johnson et al , 2017). The insufficient sequencing depth of our transcriptome data and the paucity of literature reporting on conifer ferredoxin and FNR prevented us from assessing whether epithelial cells of loblolly pine resin ducts may contain a similar arrangement of isoforms.…”

Effects of Salt Stress on Plant Growth, Antioxidant Capacity, Glandular Trichome Density, and Volatile Exudates of Schizonepeta tenuifolia Briq.

“…The EO is medicinally important since it is one of the raw materials of many Chinese Traditional Patent Medicines [ 13 ]. In the plant kingdom, there are specialized tissues and cell types responsible for synthesizing and accumulating secondary metabolites, such as secretory cavities, resin ducts, laticifers, glandular trichomes (GTs), and gum ducts [ 14 , 15 ]. While in the Lamiaceae species, the glandular trichome (GT) of the epidermal structure is the site that serves for the biosynthesis, secretion, and accumulation of EO [ 16 ].…”

Dissecting the pine tree green chemical factory

“…Therefore, these compounds are stored in specialized structures that prevent them damaging the plant itself (Lange, 2015). Examples of structures in other plant species that are similar to the resinous ducts in pine trees, as described by Turner et al , are the glandular trichomes that occur in species such as tomato (Balcke et al , 2017) and mint (Johnson et al , 2017), laticifers and oil ducts (Lange, 2015). The formation of the oleoresin constituents is not only limited to certain tissue types – to prevent toxicity – but also strictly regulated to take place only where and when they are really needed, such as under herbivore attack (Celedon et al , 2017).…”