Tandem Gene Duplication of Dioxygenases Drives the Structural Diversity of Steroidal Glycoalkaloids in the Tomato Clade

Cultivated tomato (Solanum lycopersicum) contains alpha-tomatine, a steroidal glycoalkaloid (SGA), which functions as a defense compound to protect against pathogens and herbivores; interestingly, wild species in the tomato Glade biosynthesize a variety of SGAs. In cultivated tomato, the metabolic detoxification of alpha-tomatine during tomato fruit ripening is an important trait that aided in its domestication, and two distinct 2-oxoglutarate-dependent dioxygenases (DOXs), a C-23 hydroxylase of alpha-tomatine (S123DOX) and a C-27 hydroxylase of lycoperoside C (5127DOX), are key to this process. There are tandemly duplicated DOX genes on tomato chromosome 1, with high levels of similarity to SI23DOX. While these DOX genes are rarely expressed in cultivated tomato tissues, the recombinant enzymes of Solyc01g006580 and Solyc01g006610 metabolized alpha-tomatine to habrochaitoside A and (20R)-20-hydroxytomatine and were therefore named as habrochaitoside A synthase (HAS) and cx-tomatine 20-hydroxylase (20DOX), respectively. Furthermore, 20DOX and HAS exist in the genome of wild tomato S. habrochaites accession LA1777, which accumulates habrochaitoside A in its fruits, and their expression patterns were in agreement with the SGA profiles in LA1777. These results indicate that the functional divergence of alpha-tomatinemetabolizing DOX enzymes results from gene duplication and the neofunctionalization of catalytic activity and gene expression, and this contributes to the structural diversity of SGAs in the tomato clade.

Automated summary

The metabolic detoxification of alpha-tomatine is an important trait in cultivated tomato, and two enzymes play a key role in this process. The functional divergence of these enzymes is a result of gene duplication and neofunctionalization, contributing to the structural diversity of steroidal glycoalkaloids in tomatoes.