Contribution of isopentenyl phosphate to plant terpenoid metabolism

Abstract

Plant genomes encode isopentenyl phosphate kinases (IPKs) that reactivate isopentenyl phosphate (IP) via ATP-dependent phosphorylation, forming the primary metabolite isopentenyl diphosphate (IPP) used generally for isoprenoid/terpenoid biosynthesis. Therefore, the existence of IPKs in plants raises unanswered questions concerning the origin and regulatory roles of IP in plant terpenoid metabolism. Here, we provide genetic and biochemical evidence showing that IP forms during specific dephosphorylation of IPP catalysed by a subset of Nudix superfamily hydrolases. Increasing metabolically available IP by overexpression of a bacterial phosphomevalonate decarboxylase (MPD) in Nicotiana tabacum resulted in significant enhancement in both monoterpene and sesquiterpene production. These results indicate that perturbing IP metabolism results in measurable changes in terpene products derived from both the methylerythritol phosphate (MEP) and mevalonate (MVA) pathways. Moreover, the unpredicted peroxisomal localization of bacterial MPD led us to discover that the step catalysed by phosphomevalonate kinase (PMK) imposes a hidden constraint on flux through the classical MVA pathway. These complementary findings fundamentally alter conventional views of metabolic regulation of terpenoid metabolism in plants and provide new metabolic engineering targets for the production of high-value terpenes in plants.

De novo transcriptome assembly for the five major organs of Zanthoxylum armatum and the identification of genes involved in terpenoid compound and fatty acid metabolism

“…3a), both of which utilize glycolysis to obtain the initial substrate for producing dimethylallyl diphosphate (dimethylallyl-PP). Then, dimethylallyl-PP is used to generate monoterpenoids, diterpenoids, triterpenoids, and other terpenoid compounds [14], which are the main aromatic substances involved in the special numbing taste in the fruits of Z. armatum [10]. In the present study, the results showed that almost all genes involved in terpenoid backbone biosynthesis were differentially expressed genes and detected at significant levels in the fruit samples ( Fig.…”

“…Additionally, dimethylallyl-PP can be produced via the methylerythritol phosphate (MEP) pathway. Next, isopentenyl-PP and dimethylallyl-PP are transformed into farnesyl-PP and geranyl-geranyl-PP, which are then used to produce various terpenoids, catalysed by different diphosphate synthases [14]. Fatty acids are also important productsfound in the fruit of Z. armatum.…”

The role of volatiles in plant communication

“…Also the engineering of precursor pathways is an interesting tool to alter volatile production. Intriguing work of Dudareva and co‐workers (Henry et al ., ) demonstrates an alternative role for the Nudix hydrolases that were previously shown to catalyze the first step in the formation of geraniol in rose (Magnard et al ., ). They make it likely that the Arabidopsis NUDIX1 and 3 are involved in the dephosphorylation of isopentenyl diphosphate (IPP) to isopentenyl phosphate (IP), which then serves as a substrate for isopentenyl phosphate kinase.…”

The use of mutants and inhibitors to study sterol biosynthesis in plants

“…Furthermore, it was recently shown that plants express a functional homolog of the isopentenyl phosphate kinase (IPK) that was originally identified in archaebacteria as part of their modified MVA pathway (Dellas and Noel, 2010; Henry et al , 2015). This enzyme catalyzes the phosphorylation of isopentenyl phosphate (IP) and dimethylallyl phosphate (DMAP) into IPP and DMAPP, respectively, thus increasing their availability for terpenoid production (Henry et al , 2015; Henry et al , 2018). Interestingly, IPP can be dephosphorylated back to IP by a subset of Nudix superfamily hydrolases (Henry et al, 2018).…”

“…This enzyme catalyzes the phosphorylation of isopentenyl phosphate (IP) and dimethylallyl phosphate (DMAP) into IPP and DMAPP, respectively, thus increasing their availability for terpenoid production (Henry et al , 2015; Henry et al , 2018). Interestingly, IPP can be dephosphorylated back to IP by a subset of Nudix superfamily hydrolases (Henry et al, 2018). Together, these findings illustrate the highly complex metabolic regulation of IPP and DMAPP levels for terpenoid biosynthesis in plants.…”