Metabolomic and transcriptomic analyses reveal that a MADS-box transcription factor TDR4 regulates tomato fruit quality

Authors: ZHAO, XIAODAN - Beijing Advanced Innovation Center For Food Nutrition And Human Health, Beijing Technology & Busine; YUAN, XINYU - China Agricultural University; CHEN, SHA - China Agricultural University; FU, DA-QI - China Agricultural University; Jiang, Cai-Zhong

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/31/2019
Publication Date: 6/19/2019
Citation: Zhao, X., Yuan, X., Chen, S., Fu, D., Jiang, C. 2019. Metabolomic and transcriptomic analyses reveal that a MADS-box transcription factor TDR4 regulates tomato fruit quality. Frontiers in Plant Science. 10. https://doi.org/10.3389/fpls.2019.00792.
DOI: https://doi.org/10.3389/fpls.2019.00792

Interpretive Summary: Fruit is a primary component of a healthy human diet, providing vitamins, minerals, and a wide range of bioactive compounds, including antioxidant carotenoids and various polyphenols. The key to improving fruit quality is a better understanding of the molecular mechanisms of fruit ripening. Fruit ripening is a complex biological process involving the conversion of the seed-bearing structures of fleshy fruit species into palatable and nutritious tissue that is attractive to seed dispersers. Some general ripening-associated changes are typical among fruit species, including the involvement of cell wall degradation for fruit softening, alteration of the composition and levels of secondary metabolites such as pigments, and biosynthesis of compounds for flavor and aroma development. These changes are influenced by multiple genetic and biochemical pathways that are regulated by several critical transcription factors. The tomato (Solanum lycopersicum) is one of the most important horticultural crops and is considered a good model species in the study of fleshy fruit development and ripening. In the fruits of climacteric species, including the tomato, increased ethylene production is required for the onset of ripening. During fruit development and ripening, the biosynthesis and signal transduction of ethylene are modulated by several transcription factors (TFs). A MADS-box family transcription factor TDR4 shows high sequence similarity to Arabidopsis FRUITFULL gene. In contrast to the Fruitfull TF, tomato TDR4 affects fruit ripening in an ethylene-independent manner. To further study the function of the TDR4 gene in tomato fruit ripening, in this study, we utilized virus-induced gene silencing (VIGS) to silence TDR4 expression in tomato fruit. Using transcriptomic and metabolomics approaches, we found that TDR4 functions in the metabolism of several amino acids and biosynthesis of secondary metabolites, altering fruit nutrient levels and flavor. This research provides evidence for the regulation of nutrient levels and fruit quality by tomato transcription factor TDR4.

Technical Abstract: Tomato fruit ripening is a complex process, which determines the formation of fruit quality. Many factors affect fruit ripening, including environmental conditions and genetic factors. Transcription factors (TFs) play key roles in regulating fruit ripening and quality formation. Current studies have found that the TDR4 gene is an important TF for tomato fruit ripening, but its effects on fruit metabolism and quality are less well studied. In this study, suppression of TDR4 gene expression obtained through virus-induced gene silencing (VIGS) technology resulted in an orange pericarp phenotype. Transcriptomic analysis of TDR4-silenced fruit showed changes in the expression of genes involved in various metabolic pathways, including amino acid and flavonoid biosynthesis pathways. Metabolomic analysis showed that levels of several amino acids including phenylalanine and tyrosine, and organic acids were reduced in TDR4-silenced fruit, while a-tomatine accumulated in TDR4-silenced fruit. Taken together, our RNA-seq and metabolomics analyses of TDR4-silenced fruit showed that TDR4 is involved in ripening and nutrient synthesis in tomato fruit, and is therefore an important regulator of fruit quality.