Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites

Abstract

Glandular trichomes are metabolic cell factories with the capacity to produce large quantities of secondary metabolites. Little is known about the connection between central carbon metabolism and metabolic productivity for secondary metabolites in glandular trichomes. To address this gap in our knowledge, we performed comparative metabolomics, transcriptomics, proteomics, and 13 C-labeling of type VI glandular trichomes and leaves from a cultivated (Solanum lycopersicum LA4024) and a wild (Solanum habrochaites LA1777) tomato accession. Specific features of glandular trichomes that drive the formation of secondary metabolites could be identified. Tomato type VI trichomes are photosynthetic but acquire their carbon essentially from leaf sucrose. The energy and reducing power from photosynthesis are used to support the biosynthesis of secondary metabolites, while the comparatively reduced Calvin-Benson-Bassham cycle activity may be involved in recycling metabolic CO 2 . Glandular trichomes cope with oxidative stress by producing high levels of polyunsaturated fatty acids, oxylipins, and glutathione. Finally, distinct mechanisms are present in glandular trichomes to increase the supply of precursors for the isoprenoid pathways. Particularly, the citrate-malate shuttle supplies cytosolic acetyl-CoA and plastidic glycolysis and malic enzyme support the formation of plastidic pyruvate. A model is proposed on how glandular trichomes achieve high metabolic productivity.

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

“…The carbon metabolism of glandular trichomes in Solanaceae has evolved to support high metabolite production (Balcke et al, 2017). Some genera, such as Nicotiana, produce up to 15% of their leaf biomass in the trichomes (Wagner et al, 2004).…”

Bioenergetics of Monoterpenoid Essential Oil Biosynthesis in Nonphotosynthetic Glandular Trichomes

“…In type VI GTs of Solanum habrochaites, the accumulation of terpenoids occurs over a longer period of time, while in peppermint GT, filling concludes within a matter of days (Turner et al, 2000a(Turner et al, , 2000b. Terpenoids in S. habrochaites GTs are derived from both the mevalonate and MEP pathways (Bergau et al, 2015;Balcke et al, 2017), whereas in peppermint, terpenoids of GTs are produced solely via the MEP pathway and, therefore, the reactions catalyzed by HDS and HDR (McCaskill and Croteau, 1995;Eisenreich et al, 1997;Lange et al, 2001). It is tempting to speculate that the major GT-specific Fd isoform of peppermint (and possibly other Lamiaceae) might have evolved to facilitate the particularly high flux through the reactions catalyzed by HDS and HDR en route to monoterpenoid end products.…”

Volatiles and Nonvolatiles in Flourensia campestris Griseb. (Asteraceae), How Much Do Capitate Glandular Trichomes Matter?

“…The authors have shown that sesquiterpene synthases are exclusively up regulated during the biosynthetically active stages (pre‐secretory) of the trichomes and not expressed during the post‐secretory stage. In relation to the synthesis of (–)‐HAA, an increasing number of studies have shown that terpene biosynthesis takes place within GTs . The analysis of the volatiles identified in GTs of F .…”

“…Studies from various authors reported the presence of organic acids, polysaccharides, proteins, terpenes, and phenyl compounds in GTs of several species that have been suggested to be involved in abiotic protection. Recent work from Balcke et al . in tomato, a non QAC‐accumulating species, found that glandular trichomes cope with oxidative stress by producing high levels of polyunsaturated fatty acids, oxylipins, and glutathione.…”

“…Glandular trichomes have been signaled as major production, storage and secretion sites in secondary metabolites . In the case of Flourensia , recent works by Silva et al .…”