Exploring the role of tryptamine and serotonin in tomato reproductive development

Tryptamine (TAM) and serotonin (SER) are two compounds derived from tryptophan that belong to a widespread class of bioactive molecules known as indolamines or indole alkaloids. In plants, TAM and SER are primarily recognized as intermediates in the biosynthesis of melatonin, a well-studied molecule involved in crucial biological processes such as responses to biotic and abiotic stress, reactive oxygen species (ROS) scavenging, embryo development, and plant morphogenesis. Although TAM and SER have been detected at high concentrations (μg/g of fresh weight) in the edible fruits and seeds of numerous plant species, their biological functions in reproductive organs remain unclear, and their metabolic pathways still need to be fully elucidated. The biosynthesis of TAM and SER in plants typically involves consecutive decarboxylation and hydroxylation reactions of tryptophan, catalyzed by the enzymes tryptophan decarboxylase (TDC) and tryptamine 5-hydroxylase (T5H), respectively. Our recent research has focused on the functional characterization of a three-member TDC gene family and a single T5H gene involved in the biosynthesis of TAM and SER in the model species Solanum lycopersicum. Our findings support a model in which SlTDC1 promotes TAM accumulation in fruits, SlTDC2 mediates TAM production in aerial vegetative organs, SlTDC3 drives TAM synthesis in roots and seeds, and SlT5H is responsible for the conversion of TAM to SER throughout the plant (Commisso et al., 2022). Currently, our research aims to unravel the biological functions of these two indolamines in various organs and tissues of the tomato plant. We have implemented a metabolic engineering approach, utilizing both traditional transgenesis and CRISPR/Cas9-mediated gene knockout, to generate different tomato genotypes characterized by altered levels of TAM and SER. Phenotypic characterization of SlTDC1-overexpressing lines and SlTDC1-knockout mutants revealed significant and consistent changes in the number and dimensions of ripe fruits compared to the wild-type genotype. Furthermore, seeds from sldtc1 lines exhibited altered seed coat pigmentation and a consistent reduction in germination capacity. Overall, these findings suggest a potential role for TAM and SER in reproductive development.