Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores

Abstract

Glandular trichomes are specialized hairs found on the surface of about 30% of all vascular plants and are responsible for a significant portion of a plant's secondary chemistry. Glandular trichomes are an important source of essential oils, i.e., natural fragrances or products that can be used by the pharmaceutical industry, although many of these substances have evolved to provide the plant with protection against herbivores and pathogens. The storage compartment of glandular trichomes usually is located on the tip of the hair and is part of the glandular cell, or cells, which are metabolically active. Trichomes and their exudates can be harvested relatively easily, and this has permitted a detailed study of their metabolites, as well as the genes and proteins responsible for them. This knowledge now assists classical breeding programs, as well as targeted genetic engineering, aimed to optimize trichome density and physiology to facilitate customization of essential oil production or to tune biocide activity to enhance crop protection. We will provide an overview of the metabolic diversity found within plant glandular trichomes, with the emphasis on those of the Solanaceae, and of the tools available to manipulate their activities for enhancing the plant's resistance to pests.

Figure 1

Glandular trichomes in section Lycopersicon. Wild accessions have high densities of glandular trichomes that confer resistance to several pests. Panel (A) shows the leaflet surface of Solanum habrochaites acc. LA 1777 with high densities of glandular trichome types IV and VI (B), and type I (C). Surface of Solanum pennellii acc. LA 716 is also covered by type IV trichomes (D, E) producing and secreting acyl sugars. This accession also has type VI trichomes, but in low density (F). Panel (G) shows the surface of Solanum lycopersicum cv. Moneymaker. Cultivated tomato has low density of type VI trichomes (H) and type I trichomes. Sometimes, type IV-like trichomes (I) are observed on stems, veins, and on the leaflet edges. White bars represent 500 μm in panel A, C, D, and G. In panels B, E, F, H, and I, bars represent 50 μm.

Figure 1

Glandular trichomes in section Lycopersicon. Wild accessions have high densities of glandular trichomes that confer resistance to several pests. Panel (A) shows the leaflet surface of Solanum habrochaites acc. LA 1777 with high densities of glandular trichome types IV and VI (B), and type I (C). Surface of Solanum pennellii acc. LA 716 is also covered by type IV trichomes (D, E) producing and secreting acyl sugars. This accession also has type VI trichomes, but in low density (F). Panel (G) shows the surface of Solanum lycopersicum cv. Moneymaker. Cultivated tomato has low density of type VI trichomes (H) and type I trichomes. Sometimes, type IV-like trichomes (I) are observed on stems, veins, and on the leaflet edges. White bars represent 500 μm in panel A, C, D, and G. In panels B, E, F, H, and I, bars represent 50 μm.

Figure 2

Simplified schematic overview of the biosynthesis of the main secondary metabolites stored and/or secreted by tomato glandular trichome cells. Major pathway names are shown in red, key enzymes or enzyme complexes in purple, and stored and/or secreted compounds in blue. Metabolic routes are projected onto their subcellular location, however final modification reactions (e.g., glycosylations, acylations, methylations, hydroxylations), which can take place at various organelles, are not shown for clarity. Abbreviations used: 4CL, 4-coumarate CoA ligase; ACP, acyl carrier protein; BCKD, branched-chain keto acid dehydrogenase (multi-enzyme complex); C4H, cinnamate 4-hydroxylase; CoA, coenzyme A; DMAPP, dimethylallyl diphosphate; DTS, diterpene synthase; E4P, erythrose 4-phosphate; ER, endoplasmic reticulum; FAS, fatty acid synthesis, FPP, farnesyl diphosphate; GA3P, glyceraldehyde 3-phosphate; GGPP, geranylgeranyldiphosphate; GPP, geranyldiphosphate; IPP, isopentenyl diphosphate; Leu, leucine; the non-mevalonate pathway, also known as the 2-C-methyl-D-erythritol 4-phosphate (MEP) or 1-deoxy-D-xylulose 5-phosphate (DOXP) pathway; MTS, monoterpene synthase; MVA pathway, mevalonate pathway; NPP, neryldiphosphate; PAL, phenylalanine ammonia lyase; PEP, phosphoenolpyruvate; Phe, phenylalanine; STS, sesquiterpene synthase; Val, valine. Solid black arrows indicate established biochemical reactions. Dashed black arrows indicate hypothetical reactions. A single arrow does not necessarily represent a single enzymatic conversion.