The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers

doi:10.1073/pnas.0407360102

The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers

^*Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907; and ^‡Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knoell-Strasse 8, D-07745 Jena, Germany

Edited by Rodney B. Croteau, Washington State University, Pullman, WA, and approved December 1, 2004 (received for review October 4, 2004)

Abstract

Terpenoids, the largest class of plant secondary metabolites, play essential roles in both plant and human life. In higher plants, the five-carbon building blocks of all terpenoids, isopentenyl diphosphate (IPP) and dimethylallyl diphosphate, are derived from two independent pathways localized in different cellular compartments. The methylerythritol phosphate (MEP or nonmevalonate) pathway, localized in the plastids, is thought to provide IPP and dimethylallyl diphosphate for hemiterpene, monoterpene, and diterpene biosynthesis, whereas the cytosol-localized mevalonate pathway provides C₅ units for sesquiterpene biosynthesis. Stable isotope-labeled, pathway-specific precursors (1-deoxy-[5,5-²H₂]-d-xylulose and [2,2-²H₂]-mevalolactone) were supplied to cut snapdragon flowers, which emit both monoterpenes and the sesquiterpene, nerolidol. We show that only one of the two pathways, the plastid-localized MEP pathway, is active in the formation of volatile terpenes. The MEP pathway provides IPP precursors for both plastidial monoterpene and cytosolic sesquiterpene biosynthesis in the epidermis of snapdragon petals. The trafficking of IPP occurs unidirectionally from the plastids to cytosol. The MEP pathway operates in a rhythmic manner controlled by the circadian clock, which determines the rhythmicity of terpenoid emission.

Footnotes

↵ † To whom correspondence should be addressed. E-mail: dudareva{at}hort.purdue.edu.
Author contributions: N.D., W.B., and J.G. designed research; N.D., S.A., and I.O. performed research; N.G. contributed new reagents/analytic tools; N.D., I.O., M.R., D.R., and J.G. analyzed data; and N.D., S.A., N.G., M.R., D.R., W.B., and J.G. wrote the paper.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations: IPP, isopentenyl diphosphate; DMAPP, dimethylallyl diphosphate; MVA, mevalonic acid; MVL, racemic [2,2-²H₂]-mevalolactone; MEP, methylerythritol phosphate; GPP, geranyl diphosphate; DOX, 1-deoxy-d-xylulose; DXP, 1-deoxy-d-xylulose-5-phosphate; DXPS, DXP synthase; DXR, 1-deoxy-d-xylulose-5-phosphate reductoisomerase; HMGR, 3-hydroxy-3-methylglutaryl-CoA reductase; amu, atomic mass units.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. AY770406 (for snapdragon DXR gene) and AY770407 (for snap-dragon DXPS gene)].