High-level sesquiterpene-production in tomato glandular trichomes

Type-VI glandular trichomes of wild tomato Solanum habrochaites PI127826 produce high levels of the sesquiterpene 7-epizingiberene and its derivatives, making the plant both repellent and toxic to several pest insects and pathogens. How wild tomato trichomes achieve such high terpene production is still largely unknown.. Here we show that a cross (F1) with a cultivated tomato S. lycopersicum produced only minute levels of 7-epizingiberene. In the F2-progeny, selected for the presence of the 7-epizingiberene biosynthesis genes, only three percent produced comparable amounts the wild parent, indicating this trait is recessive and multigenic. Morevoer, high production did not correlate with trichome density. We selected F2 plants with the “high-production active-trichome phenotype” of PI127826, producing about 150 times higher levels of terpenes than F2 individuals that displayed a “low-production lazy-trichome phenotype”. The quantity terpenes in trichomes of these F2 plants correlated with the volume of the storage cavity and the gland shape. We found that trichome morphology is not a predetermined characteristic, but cavity size rather depended on gland-cell metabolic activity. Inhibitor assays showed that the plastidial-precursor pathway (MEP) is fundamental for high-level production of both cytosolic as well as plastid-derived terpenes in tomato trichomes. Gene-expression profiles of isolated secretory cells showed that key-enzymes in the MEP pathway were higher expressed in active trichomes . We conclude that the MEP pathway is the primary precursor supply route in wild type-VI trichomes and that the high-production phenotype of the wild tomato trichome is indeed a multigenic trait.