Specialized Metabolites and Related Biosynthetic Enzymes in Tomato Glandular Trichomes: Defining Biological Functions of Specific Gland Types.

Abstract

Trichomes are tiny appendages that grow out from the surfaces of leaves, stems, flowers, and other above-ground parts of many plants. They contribute to important biological functions such as determent of herbivores, attraction of pollinators, and protection against abiotic stresses. Comparisons of glandular trichome-derived specialized metabolites from wild and cultivated tomato species have revealed that the ability to synthesize many of the defensive specialized metabolites has been lost during the process of domestication. Reintroduction of such traits into the cultivated tomato may prove to be an effective way of reducing crop loss and dependence on pesticides. We investigated the different types of glandular trichomes present on the leaf surface of several different wild tomato species and on cultivated tomato by metabolite profiling and gene transcript profiling of the gland cells. Substantial differences within and between species and glandular trichome types were found for acyl-sugars, terpenoids, and flavonoids. Gene transcripts required for the synthesis of these classes of specialized metabolites were found in the gland cells of type 1, 4, and type 6 glandular trichomes. In an in-depth study of one class of metabolites, we found that the wild tomato species, S. habrochaites, accumulates highly methylated derivatives of myricetin, a flavonol, in the glandular trichomes. Using collections of gland cells from the different glandular trichome types, we showed that secreting glandular trichomes (designated type 1 and 4) contained several-fold more of these compounds than storage glandular trichomes (type 6). We also identified transcripts of two genes expressed in the glandular trichomes, designated ShMOMT1 (Solanum habrochaites myricetin O-methyltransferase) and ShMOMT2, and showed that they encode enzymes capable of methylating myricetin at the 3′ and 5′ and the 7 and 4′ positions, respectively. Both genes are preferentially expressed in secreting glandular trichome types 1 and 4, and to a lesser degree in storage trichome type 6, and ShMOMT1 and ShMOMT2 protein levels are correspondingly higher in type 1 and 4 glands compared with type 6 glands.