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Functional identification and differential expression of 1-deoxy-d-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies)

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Abstract

Conifers produce terpenoid-based oleoresins as constitutive and inducible defenses against herbivores and pathogens. Much information is available about the genes and enzymes of the late steps of oleoresin terpenoid biosynthesis in conifers, but almost nothing is known about the early steps which proceed via the methylerythritol phosphate (MEP) pathway. Here we report the cDNA cloning and functional identification of three Norway spruce (Picea abies) genes encoding 1-deoxy-d-xylulose 5-phosphate synthase (DXS), which catalyzes the first step of the MEP pathway, and their differential expression in the stems of young saplings. Among them are representatives of both types of plant DXS genes. A single type I DXS gene is constitutively expressed in bark tissue and not affected by wounding or fungal application. In contrast, two distinct type II DXS genes, PaDXS2A and PaDXS2B, showed increased transcript abundance after these treatments as did two other genes of the MEP pathway tested, 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR) and 4-hydroxyl 3-methylbutenyl diphosphate reductase (HDR). We also measured gene expression in a Norway spruce cell suspension culture system that, like intact trees, accumulates monoterpenes after treatment with methyl jasmonate. These cell cultures were characterized by an up-regulation of monoterpene synthase gene transcripts and enzyme activity after elicitor treatment, as well as induced formation of octadecanoids, including jasmonic acid and 12-oxophytodienoic acid. Among the Type II DXS genes in cell cultures, PaDXS2A was induced by treatment with chitosan, methyl salicylate, and Ceratocystis polonica (a bark beetle-associated, blue-staining fungal pathogen of Norway spruce). However, PaDXS2B was induced by treatment with methyl jasmonate and chitosan, but was not affected by methyl salicylate or C. polonica. Our results suggest distinct functions of the three DXS genes in primary and defensive terpenoid metabolism in Norway spruce.

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Acknowledgements

We thank Kerstin Manke (IPB, Halle) for skillful technical assistance, Xue Mei Niu (Hans Knöll Institute, Jena) for the preparation of C. polonica spore cultures and Ms. Sharon Jancsik (UBC Michael Smith Laboratories) for maintaining the EST/FLcDNA-collections of the TREENOMIX:Conifer Forest Health Project. We also thank Paal Krokene of the Norwegian Forest Research Institute (Ås, Norway), for providing the C. polonica strain. The research reported in this paper was supported with funds from the Max Planck Society (to JG), Genome British Columbia and Genome Canada in support of the TREENOMIX:Conifer Forest Health Project (grant to JB), and the Natural Sciences and Engineering Council of Canada (NSERC, grant to JB). JB is an NSERC E.W.R. Steacie Memorial fellow.

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Authors and Affiliations

  1. Max Planck Institut für Chemische Ökologie, Abteilung Biochemie, Hans Knöll Str. 8, Jena, 07745, Germany

    Michael A. Phillips, Katrin Luck & Jonathan Gershenzon

  2. Leibniz-Institut für Pflanzenbiochemie, Abteilung Sekundärstoffwechsel, Weinberg 3, Halle (Saale), 06120, Germany

    Michael H. Walter & Dieter Strack

  3. Michael Smith Laboratories, University of British Columbia, Vancouver, Canada

    Steven G. Ralph & Jörg Bohlmann

  4. Max Planck Institut für Chemische Ökologie, Abteilung Bioorganische Chemie, Hans Knöll Str. 8, Jena, 07745, Germany

    Paulina Dabrowska & Wilhelm Boland

  5. Departament de Bioquímica i Biología Molecular, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, 08282, Barcelona, Spain

    Eva Maria Urós & Manuel Rodríguez-Concepción

  6. Consorci CSIC-IRTA de Genetica Molecular Vegetal, Jordi Girona 18-26, 08034, Barcelona, Spain

    Eva Maria Urós & Manuel Rodríguez-Concepción

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  1. Michael A. Phillips
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Phillips, M.A., Walter, M.H., Ralph, S.G. et al. Functional identification and differential expression of 1-deoxy-d-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol 65, 243–257 (2007). https://doi.org/10.1007/s11103-007-9212-5

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