HDR, the last enzyme in the MEP pathway, differently regulates isoprenoid biosynthesis in two woody plants

Dimethylallyl diphosphate (DMADP) and isopentenyl diphosphate (IDP) serves as the universal C-5 precursors of isoprenoid biosynthesis in plants. These compounds are formed by the last step of the 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway, catalyzed by (E)-4-hydroxy-3-methylbut-2-en-1-yl diphosphate reductase (HDR). In this study, we investigated the major HDR isoforms of two woody plant species, Norway spruce (Picea abies) and gray poplar (Populus x canescens), to determine how they regulate isoprenoid formation. Since each of these species has a distinct profile of isoprenoid compounds, they may require different proportions of DMADP and IDP with proportionally more IDP being needed to make larger isoprenoids. Norway spruce contained two major HDR isoforms differing in their occurrence and biochemical characteristics. PaHDR1 produced relatively more IDP than PaHDR2 and it encoding gene was expressed constitutively in leaves, likely serving to form substrate for production of carotenoids, chlorophylls, and other primary isoprenoids derived from a C-20 precursor. On the other hand, Norway spruce PaHDR2 produced relatively more DMADP than PaHDR1 and its encoding gene was expressed in leaves, stems, and roots, both constitutively and after induction with the defense hormone methyl jasmonate. This second HDR enzyme likely forms a substrate for the specialized monoterpene (C-10), sesquiterpene (C-15), and diterpene (C-20) metabolites of spruce oleoresin. Gray poplar contained only one dominant isoform (named PcHDR2) that produced relatively more DMADP and the gene of which was expressed in all organs. In leaves, where the requirement for IDP is high to make the major carotenoid and chlorophyll isoprenoids derived from C-20 precursors, excess DMADP may accumulate, which could explain the high rate of isoprene (C-5) emission. Our results provide new insights into the biosynthesis of isoprenoids in woody plants under conditions of differentially regulated biosynthesis of the precursors IDP and DMADP. Isoprenoid biosynthesis in woody plants with a distinct profile of isoprenoid compounds is regulated by the ratio of the precursors isopentenyl diphosphate and dimethylallyl diphosphate.

Automated summary

This study investigated the major HDR isoforms in Norway spruce and gray poplar to determine their regulation of isoprenoid formation. The results showed that Norway spruce has two different HDR isoforms, with one producing more IDP for carotenoid and chlorophyll production, and the other producing more DMADP for specialized metabolites. Gray poplar, on the other hand, has only one dominant isoform that produces more DMADP, potentially explaining its high rate of isoprene emission.