Abstract
The shoot system of pines contains abundant resin ducts, which harbor oleoresins that play important roles in constitutive and inducible defenses. In a pilot study, we assessed the chemical diversity of oleoresins obtained from mature tissues of loblolly pine trees (Pinus taeda L.). Building on these data sets, we designed experiments to assess oleoresin biosynthesis in needles of 2-year-old saplings. Comparative transcriptome analyses of single cell types indicated that genes involved in the biosynthesis of oleoresins are significantly enriched in isolated epithelial cells of resin ducts, compared with those expressed in mesophyll cells. Simulations using newly developed genome-scale models of epithelial and mesophyll cells, which incorporate our data on oleoresin yield and composition as well as gene expression patterns, predicted that heterotrophic metabolism in epithelial cells involves enhanced levels of oxidative phosphorylation and fermentation (providing redox and energy equivalents). Furthermore, flux was predicted to be more evenly distributed across the metabolic network of mesophyll cells, which, in contrast to epithelial cells, do not synthesize high levels of specialized metabolites. Our findings provide novel insights into the remarkable specialization of metabolism in epithelial cells.
Highlights
Oleoresins form constitutively and abundantly in the stems and needles of many conifers
Comparative transcriptome analyses of single cell types indicated that genes involved in the biosynthesis of oleoresins are significantly enriched in isolated epithelial cells of resin ducts, compared with those expressed in mesophyll cells
Most genes known to be involved in oleoresin biosynthesis were highly enriched in the three replicate transcriptomes of epithelial cells compared with those obtained from mesophyll cell).The expression levels of these genes in mesophyll cells was generally at a level that could be explained by cross-contamination from neighboring epithelial cells.The exceptions were two genes coding for putative sesquiterpene synthases, for which transcript abundance was higher in mesophyll cells than would be expected from epithelial cell contamination (Fig. 3)
Summary
Oleoresins form constitutively and abundantly in the stems and needles of many conifers. They can be synthesized and secreted as an induced defensive response to herbivore or pathogen attack (Franceschi et al, 2005; Keeling and Bohlmann, 2006).The stems of the genera Abies, Cedrus, Tsuga, and Pseudolarix accumulate oleoresins constitutively in sac-like structures called resin blisters, whereas Pinus, Picea, Larix, and Pseudotsuga resins are found in tubular networks of ducts (Fahn, 1988).Wounding and methyl jasmonate treatment can elicit the formation of resin ducts even in conifer species that normally lack ducts (Hudgins and Franceschi, 2004). The chemistry of conifer oleoresins is characterized by mixtures of volatiles (primarily monoterpenes) and semi-volatiles (primarily diterpenoids) (Joye and Lawrence, 1967; Norin, 1972) (Fig. 1). Oleoresins, which are characterized by a high volumetric energy density and high 218 | Turner et al
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