Abstract

In response to changing environments, plants regulate gene expression and subsequent metabolism to acclimate and survive. A superfamily of acyl-activating enzymes (AAEs) has been observed in every class of creatures on planet. Some of plant AAE genes have been identified and functionally characterized to be involved in growth, development, biotic, and abiotic stresses via mediating diverse metabolic pathways. However, less information is available about AAEs superfamily in tomato (Solanum lycopersicum), the highest value fruit and vegetable crop globally. In this study, we aimed to identify tomato AAEs superfamily and investigate potential functions with respect to aluminum (Al) stress that represents one of the major factors limiting crop productivity on acid soils worldwide. Fifty-three AAE genes of tomato were identified and named on the basis of phylogenetic relationships between Arabidopsis and tomato. The phylogenetic analysis showed that AAEs could be classified into six clades; however, clade III contains no AAE genes of tomato. Synteny analyses revealed tomato vegetable paralogs and Arabidopsis orthologs. The RNA-seq and quantitative reverse-transcriptase PCR (qRT-PCR) analysis indicated that 9 out of 53 AAEs genes were significantly up- or downregulated by Al stress. Numerous cis-acting elements implicated in biotic and abiotic stresses were detected in the promoter regions of SlAAEs. As the most abundantly expressed gene in root apex and highly induced by Al, there are many potential STOP1 cis-acting elements present in the promoter of SlAAE3-1, and its expression in root apex was specific to Al. Finally, transgenic tobacco lines overexpressing SlAAE3-1 displayed increased tolerance to Al. Altogether, our results pave the way for further studies on the functional characterization of SlAAE genes in tomato with a wish of improvement in tomato crop in the future.

Highlights

  • Aluminum (Al) toxicity is one of the major limiting factors affecting the crop productivity in acidic soils, which occupy nearly 50% of the potential arable lands of the world (von Uexküll and Mutert, 1995)

  • To confirm that the identified differentially expressed SlAAE genes are exactly involved in tolerance to stresses, we developed transgenic tobacco lines overexpressing SlAAE3-1 that is most significantly induced by Al in the tomato root apex

  • We further divided tomato activating enzymes (AAEs) superfamily into five distinct clades based on the phylogenetic analysis (Figure 1)

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Summary

Introduction

Aluminum (Al) toxicity is one of the major limiting factors affecting the crop productivity in acidic soils, which occupy nearly 50% of the potential arable lands of the world (von Uexküll and Mutert, 1995). The initial and most visible symptom of Al toxicity is inhibition of root elongation by ravaging cell structure of the root apex and limiting the mineral nutrient and water uptake and, hindering the plant growth and development (Kochian, 1995; Ma, 2007; Ryan et al, 2011; Liu et al, 2014). To adapt to Al-toxic environment, plants have evolved two major types of Al-tolerance mechanisms, namely, external exclusion (preventing Al from entering cells of root apex) and internal tolerance mechanisms (detoxifying Al via complexation and sequestration) (Kochian et al, 2004, 2015; Liu et al, 2014). The molecular basis of the role of metabolic alterations in Al stress response still needs further elucidation

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