The Bittersweet Symphony: Characterization of GORKY, the Novel Steroidal Glycoalkaloid Transporter

Steroidal alkaloids are specialized metabolites present in the Solanaceae family, where they play an important role in plant defense against pathogens and predators. When consumed, high concentrations of steroidal glycoalkaloids in food are associated with bitter taste and burning sensation in the throat. α-tomatine is the main steroidal glycoalkaloid present in tomato plants, accumulating in early stage green fruit, leaves and flower buds. However, during tomato fruit ripening α-tomatine levels drastically decrease and its entire pool is converted to hydroxylated, glycosylated and acylated non-bitter forms termed esculeosides and lycoperosides. Nevertheless, wild accessions exist, that display high levels of α-tomatine in fully ripe fruits similar to the wild tomato species. Here we present the discovery of GORKY, a novel nitrate/peptide family (NPF) transporter that exports α-tomatine and other steroidal alkaloids from the vacuole to the cytosol, where they are further metabolized during fruit ripening.

Functional characterization of GORKY, its localization and transport activity indicates that it plays a pivotal role in re-compartmentalization of α-tomatine and possibly other steroidal alkaloids during ripening that facilitates the conversion of the entire pool of α-tomatine to hydroxylated, glycosylated and acylated non-bitter forms rendering the fruits more palatable.

Our results suggest that GORKY activity was a significant innovation in the process of tomato fruit evolution.