The transcription factor AREB1 regulates primary metabolic pathways in tomato fruits

Adriana Bastías,José A. Casaretto,Aurelio Gómez-Cadenas,Alisdair R. Fernie,Vicent Arbona,Sonia Osorio,Mónica Yañez

doi:10.1093/jxb/eru114

Abstract

Tomato fruit development is regulated both by the action of plant hormones and by tight genetic control. Recent studies suggest that abscisic acid (ABA) signalling may affect different aspects of fruit maturation. Previously, it was shown that SlAREB1, an ABA-regulated transcription factor involved in stress-induced responses, is expressed in seeds and in fruit tissues in tomato. Here, the role of SlAREB1 in regulating the expression of genes relevant for primary metabolic pathways and affecting the metabolic profile of the fruit was investigated using transgenic tomato lines. Metabolite profiling using gas chromatography-time of flight mass spectrometry (GC-TOF-MS) and non-targeted liquid chromatography-mass spectrometry (LC-MS) was performed on pericarp tissue from fruits harvested at three stages of fruit development. Principal component analysis of the data could distinguish the metabolite profiles of non-transgenic fruits from those that overexpress and down-regulate SlAREB1. Overexpression of SlAREB1 resulted in increased content of organic acids, hexoses, hexose-phosphates, and amino acids in immature green, mature green, and red ripe fruits, and these modifications correlated with the up-regulation of enzyme-encoding genes involved in primary carbohydrate and amino acid metabolism. A non-targeted LC-MS analysis indicated that the composition of secondary metabolites is also affected in transgenic lines. In addition, gene expression data revealed that some genes associated with fruit ripening are also up-regulated in SlAREB1-overexpressing lines compared with wild-type and antisense lines. Taken together, the results suggest that SlAREB1 participates in the regulation of the metabolic programming that takes place during fruit ripening and that may explain part of the role of ABA in fruit development in tomato.

Highlights

Tomato is the most widespread and the most important horticultural crop worldwide and is the most widely used model to study different aspects of fruit development
The results indicate that SlAREB1 affects the content of amino acids, organic acids, and sugar derivatives most probably by regulating the expression of enzyme-encoding genes involved in primary carbohydrate and amino acid metabolic pathways, suggesting that this transcription factor mediates an abscisic acid (ABA) signal that may be relevant for the regulation of the metabolic programming that takes place during fruit ripening in tomato
Previous analysis of the main organic acids associated with organoleptic attributes of mature fruits suggested that expression of SlAREB1 affects the concentrations of citrate, malate, and glutamate as well as those of fructose and glucose (Bastías et al, 2011)

Summary

Introduction

Tomato is the most widespread and the most important horticultural crop worldwide and is the most widely used model to study different aspects of fruit development. Transcriptomic and proteomic approaches have been used to identify genetic networks of specific processes during fruit growth, such as fruit setting, early fruit tissue specialization, development of tomato fruit surface tissues, and ripening (Alba et al, 2005; Rocco et al, 2006; Mintz-Oron et al, 2008; Vriezen et al, 2008; Osorio et al, 2011). These analyses have revealed a clear participation of enzymes, regulatory proteins, and hormonal signals in both primary and secondary metabolism. Research on a link between hormonal signals that participate during this transition period and the control of gene expression involved in the modulation of metabolism is still ongoing

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