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Review
, 175 (1), 6-22

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

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Review

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

Alexandre Huchelmann et al. Plant Physiol.

Abstract

Multicellular glandular trichomes are epidermal outgrowths characterized by the presence of a head made of cells that have the ability to secrete or store large quantities of specialized metabolites. Our understanding of the transcriptional control of glandular trichome initiation and development is still in its infancy. This review points to some central questions that need to be addressed to better understand how such specialized cell structures arise from the plant protodermis. A key and unique feature of glandular trichomes is their ability to synthesize and secrete large amounts, relative to their size, of a limited number of metabolites. As such, they qualify as true cell factories, making them interesting targets for metabolic engineering. In this review, recent advances regarding terpene metabolic engineering are highlighted, with a special focus on tobacco (Nicotiana tabacum). In particular, the choice of transcriptional promoters to drive transgene expression and the best ways to sink existing pools of terpene precursors are discussed. The bioavailability of existing pools of natural precursor molecules is a key parameter and is controlled by so-called cross talk between different biosynthetic pathways. As highlighted in this review, the exact nature and extent of such cross talk are only partially understood at present. In the future, awareness of, and detailed knowledge on, the biology of plant glandular trichome development and metabolism will generate new leads to tap the largely unexploited potential of glandular trichomes in plant resistance to pests and lead to the improved production of specialized metabolites with high industrial or pharmacological value.

Figures

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Figure 1.
Figure 1.
Glandular trichome initiation and development, a process with many unknowns. A differentiating protodermal cell integrates both environmental and endogenous signals. Such signal integration results in the selection of a pool of trichome cell precursors that will initiate a specific developmental program. In these trichome initials, cell-specific transcriptional control of gene expression and cell cycle regulation results in the onset of a controlled cell division and trichome morphogenesis program, most of which is still not so well understood in the case of glandular trichomes. It probably also involves some cell-cell signaling promoting the one cell-spacing rule, which allows a specific patterning of trichomes in the epidermis. Morphogenesis of the trichome glandular head also necessitates extensive remodeling of the cell wall. The extent of endoreduplication in glandular trichomes is still mostly uncharacterized. The illustration shows a modified confocal image of a long glandular trichome initial from N. tabacum. Chloroplasts are shown in green, propidium iodide-stained cell walls in magenta, and nuclei in cyan.
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Figure 2.
Figure 2.
Glandular trichome initiation and development in N. tabacum. A to F, Confocal microscopy images showing the early steps of glandular trichome development. The number of cells forming the developing glandular trichome is shown at the bottom of each frame. A differentiating protodermal cell enlarges and forms a protuberance (A), the cell nucleus migrates to the tip of the protuberance (B), and cell division takes place (C), forming a structure made of two cells (D). The upper cell protruding from the epidermis then undergoes an asymmetric division, forming one large cell (which will form the multicellular stalk after several rounds of controlled cell division) and one small cell (which will give rise to the multicellular glandular head; E). A developing trichome made of five cells is shown in F. Scale bars, 20 μm. Magenta represents cell wall (propidium iodide staining), cyan represents nuclei (4',6-Diamidine-2'-phenylindole staining), and green represents chloroplasts (chlorophyll a autofluorescence). G, Scanning electron micrograph showing the typical cell architecture of a mature long glandular trichome.
Figure 3.
Figure 3.
Isoprenoid metabolism in N. tabacum cells. The red square represents the major MEP isoprenoid metabolism in plastids of developed trichomes. Phytohormones are indicated in blue and specialized metabolites in violet. ABA, Abscisic acid; FPP, farnesyl diphosphate; GGPP, geranylgeranyl diphosphate; GPP, geranyl diphosphate.
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Figure 4.
Figure 4.
Terpenoid metabolism in engineered tobacco trichomes for triterpene production in the cytosol. The gray pathway represents the normal biosynthetic route for triterpenes and sterols. The enzymes are targeted to the cytosol to enhance the cross talk and sink the plastids from its precursors. Overexpressed enzymes are denoted in dark blue. New products deriving from the engineering metabolism are denoted in light blue. CYP450, Cytochrome P450; FDS, farnesyl diphosphate synthase; FPP, farnesyl diphosphate; GGPP, geranylgeranyl diphosphate; GPP, geranyl diphosphate; OSC, 2,3-oxidosqualene cyclase; SQE, squalene epoxidase; SQS, squalene synthase.
Figure 5.
Figure 5.
Terpenoid metabolism in engineered tobacco trichomes for triterpene production in plastids. The gray pathway represents the normal biosynthetic route for triterpenes and sterols. The enzymes are targeted to directly produce the triterpenes in the plastids. Overexpressed enzymes are denoted in dark blue. New products deriving from the engineering metabolism are denoted in light blue. The sinking plastidial isoprenoid pool might provoke undesirable consequences. Potentially affected metabolites are denoted in orange. ABA, Abscisic acid; CYP450, cytochrome P450; FDS, farnesyl diphosphate synthase; FPP, farnesyl diphosphate; GGPP, geranylgeranyl diphosphate; GPP, geranyl diphosphate; OSC, 2,3-oxidosqualene cyclase; SQE, squalene epoxidase; SQS, squalene synthase.
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