In search of tryptamine and serotonin biological roles in tomato

Tryptamine and serotonin are two indolamines which presence was recently reported in many plant species and emerging reports suggest the ubiquity of these molecules in the whole plant kingdom. The occurrence of these metabolites obviously reflect the existence of a biosynthetic route involved in their production and the first gene codifying for a tryptophan decarboxylase (TDC), able to convert the amino acid tryptophan into tryptamine, was characterized from Catharanthus roseus. In this plant species, tryptamine is sequestered into the vacuole and there directed in the biosynthesis of indolalkaloids. On the other hand, tryptamine can be directed in the production of serotonin in other plant species, as demonstrated for Oryza sativa plants. Indeed, tryptamine is turned into serotonin through the action of a Tryptamine 5-Hydroxylase (T5H) enzyme. In rice, both tryptamine and serotonin are believed to be directed in the production of melatonin through the action of other two enzymes. N-acetyltransferase (SNAT) and N-acetylserotonin methyltransferase (ASMT) are indeed responsible for the conversion of serotonin into N-acetylserotonin and finally melatonin, respectively. However, the occurrence of high levels of tryptamine and serotonin and their derivatives, especially esters linked with hydroxycinnamate moieties, in rice and other plant species suggest that these two indolamines might be final product rather than mere precursors of indolalkaloids or melatonin. Moreover, it has been reported that O. sativa plants has three genes coding for TDCs and this arises the hypothesis that TDC product might display multiple biological roles. Beside the well-known neurotransmitter activity exerted in animals, serotonin was demonstrated to be involved in the protection of rice leaves against biotic stressors, such as the fungus Bipolaris oryzae and Magnaportea grisea. On the contrary, little is known about the role of tryptamine in plants, except for some evidences derived from experiments on plants overexpressing C. roseus TDC, where the high presence of tryptamine in the leaves negatively affected insect reproduction. During a previous project focused in the metabolome characterization of fruits from several plant species and cultivars, we found high levels of tryptamine and serotonin in methanolic extracts of Actinidia spp. and Solanum lycorpesicum. Since the previously mentioned roles were observed in plants that mainly accumulate tryptamine and serotonin in leaves, we focused about the biological role played by these indolamines in fleshy fruits. In this project, S. lycopersicum L. cv MicroTom plants were used as model plant species and the transient heterologous transformation of Nicotiana benthamiana plants, which do not usually accumulate tryptamine nor serotonin, allowed us to characterize three different tomato TDCs and one T5H genes. Moreover, we observed a specific and precise spatial distribution of tryptamine and serotonin in different tomato tissues and organs, including a gradient of accumulation along the plant stem, suggesting a fine regulation of metabolite production and/or translocation. Acknowledgements: this project was funded by Regione Veneto.