Role of the tomato TAGL1 gene in regulating fruit metabolites elucidated using RNA sequence and metabolomics analyses.

Xiaodan Zhao,Daqi Fu,Sha Chen,Lanhuan Meng,Xinyu Yuan,Marie-Joelle Virolle

doi:10.1371/journal.pone.0199083

Abstract

Fruit ripening is a complex biological process affecting fruit quality. In tomato the fruit ripening process is delicately regulated by transcription factors (TFs). Among these, the TOMATO AGAMOUS-LIKE 1 (TAGL1) gene plays an important role in both the development and ripening of fruit. In this study, the TAGL1 gene was successfully silenced by virus-induced gene silencing technology (VIGS), and the global gene expression and metabolites profiles of TAGL1-silenced fruits were analyzed by RNA-sequence analysis (RNA-seq) and liquid chromatography–mass spectrometry (LC-MS/MS). The TAGL1-silenced fruits phenotypically displayed an orange pericarp, which was in accordance with the results expected from the down-regulation of genes associated with carotenoid synthesis. Levels of several amino acids and organic acids were lower in the TAGL1-silenced fruits than in the wild-type fruits, whereas, α-tomatine content was greatly increased (more than 10-fold) in the TAGL1-silenced fruits compared to wild-type fruits. The findings of this study showed that TAGL1 not only regulates the ripening of tomato fruits, but also affects the synthesis and levels of nutrients in the fruit.

Highlights

Fruit ripening is a complex developmental process that involves the transformation of the seed-bearing structure of fleshy fruit species into a delicious and nutritive fruit, which appeals to animals and humans, who consume the fruit and act as the dispersers of its seeds [1]
In order to obtain TOMATO AGAMOUS-LIKE 1 (TAGL1)-silenced tomato fruit by virusinduced gene silencing technology (VIGS), Agrobacterium GV3101 cultures containing either pTRV1: pTRV2-TAGL1 or pTRV1 and pTRV2-00 were injected into the carpopodium of the tomato fruit 7–10 day post-anthesis (DPA) after pollination and fruit phenotypes were observed 20–30 days after injection
The result reveals that the down-regulation of TAGL1 causes the unusual ripening phenotype of tomato fruits, which was consistent with the previous finding that TAGL1-RNAi fruits were yellow-orange upon ripening [15, 16]

Summary

Introduction

Fruit ripening is a complex developmental process that involves the transformation of the seed-bearing structure of fleshy fruit species into a delicious and nutritive fruit, which appeals to animals and humans, who consume the fruit and act as the dispersers of its seeds [1]. Some general ripening-associated changes are characteristic among different species, including modifications in texture, changes in the sugar content, and alterations in the composition and levels of secondary metabolites such as pigments and flavor [2, 3]. These changes are associated with alterations in multiple biochemical pathways that are regulated by some critical TFs [4, 5]. Tomato (Solanum lycopersicum), one of the world’s most important horticultural crops and an important source of human nutrients, is recognized as an outstanding experimental model to study fleshy fruit development and ripening [3, 4].

Methods

Results

Conclusion