Unraveling the mystery of the roles of tryptamine and serotonin in Solanum lycopersicum

Plants produce a vast array of small molecules, called specialized metabolites, in response to various physiological and ecological stimuli. Despite the rich arsenal of techniques available, the biological roles of many plant metabolites still remain uncovered, and, in this context, several efforts have been made to unravel the functions of the indolamines tryptamine (TAM) and serotonin (SER). The biosynthetic pathway involving TAM and SER in plants starts with the decarboxylation of tryptophan by tryptophan decarboxylase (TDC) to produce TAM, which is, in turn, converted into SER by tryptamine 5-hydroxylase (T5H). TAM and SER have been identified as intermediates in the biosynthesis of melatonin; however, the very high values of TAM and SER in plants (μg/g of fresh weight), especially in the edible fruits and seeds of important crops, such as tomato, suggest that they have specific biological roles in the reproductive organs. To study the biological roles of TAM and SER in Solanum lycopersicum, we previously characterized a three-member TDC gene family and a single T5H gene. Moreover, after combining gene expression levels with indolamine contents in tomato tissues and organs, we proposed a model where SlTDC1 and SlTDC2 promote TAM accumulation in fruits and aerial vegetative organs, respectively. SlTDC3 drives TAM synthesis in roots and seeds, and SlT5H catalyzes the conversion of TAM to SER throughout the plant. A metabolic engineering approach involving both conventional transgenesis and CRISPR/Cas9-mediated gene knockout was employed to generate tomato lines with altered TAM and SER levels. Phenotypic analysis of SlTDC1-overexpressing and knockout lines revealed notable changes in fruit size and number compared to the wild-type line. Additionally, seeds from the SlTDC1 knockout lines exhibited altered seed coat pigmentation and reduced germination rates. These observations suggest that TAM and SER may play critical roles in the reproductive development of the tomato plant.