Abstract

Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is an important vegetable crop world-wide. Watermelon fruit quality is a complex trait determined by various factors such as sugar content, flesh color and flesh texture. Fruit quality and developmental process of cultivated and wild watermelon are highly different. To systematically understand the molecular basis of these differences, we compared transcriptome profiles of fruit tissues of cultivated watermelon 97103 and wild watermelon PI296341-FR. We identified 2,452, 826 and 322 differentially expressed genes in cultivated flesh, cultivated mesocarp and wild flesh, respectively, during fruit development. Gene ontology enrichment analysis of these genes indicated that biological processes and metabolic pathways related to fruit quality such as sweetness and flavor were significantly changed only in the flesh of 97103 during fruit development, while those related to abiotic stress response were changed mainly in the flesh of PI296341-FR. Our comparative transcriptome profiling analysis identified critical genes potentially involved in controlling fruit quality traits including α-galactosidase, invertase, UDP-galactose/glucose pyrophosphorylase and sugar transporter genes involved in the determination of fruit sugar content, phytoene synthase, β-carotene hydroxylase, 9-cis-epoxycarotenoid dioxygenase and carotenoid cleavage dioxygenase genes involved in carotenoid metabolism, and 4-coumarate:coenzyme A ligase, cellulose synthase, pectinesterase, pectinesterase inhibitor, polygalacturonase inhibitor and α-mannosidase genes involved in the regulation of flesh texture. In addition, we found that genes in the ethylene biosynthesis and signaling pathway including ACC oxidase, ethylene receptor and ethylene responsive factor showed highly ripening-associated expression patterns, indicating a possible role of ethylene in fruit development and ripening of watermelon, a non-climacteric fruit. Our analysis provides novel insights into watermelon fruit quality and ripening biology. Furthermore, the comparative expression profile data we developed provides a valuable resource to accelerate functional studies in watermelon and facilitate watermelon crop improvement.

Highlights

  • Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is an important vegetable crop in the Cucurbitaceae family with sweet and juicy fruit containing high content of lycopene [1]

  • We identified a total of 16 ethylene responsive factor (ERF) genes that were differentially expressed during fruit development and ripening and these ERFs genes showed distinct expression patterns in the cultivated and wild watermelon (S11 Table)

  • Genome-wide comparative gene expression analysis between the cultivated and wild watermelon would provide a better understanding of the genetic bases contributing to the differences of their fruit development

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Summary

Introduction

Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is an important vegetable crop in the Cucurbitaceae family with sweet and juicy fruit containing high content of lycopene [1]. The fruits of cultivated and wild watermelon undergo highly different biochemical and physiological changes such as sugar and pigment accumulation, fruit softening, and changes of flavor and aromatic volatile contents [1, 5], all of which are caused by developmentally and physiologically changes in gene expression profiles. These differences provide an ingenious system to discover molecular mechanisms and candidate genes governing the process of fruit quality development. Gene expression profiles during fruit development in wild watermelon have not been investigated

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