Identification of key gene networks controlling organic acid and sugar metabolism during watermelon fruit development by integrating metabolic phenotypes and gene expression profiles

Muhammad Jawad Umer,Hongju Zhu,Haileslassie Gebremeskel,Wenge Liu,Luqman Bin Safdar,Muhammad Anees,Nan He,M O Kaseb,Pingli Yuan,Xuqiang Lu,Chengsheng Gong,Shengjie Zhao

doi:10.1038/s41438-020-00416-8

Abstract

The organoleptic qualities of watermelon fruit are defined by the sugar and organic acid contents, which undergo considerable variations during development and maturation. The molecular mechanisms underlying these variations remain unclear. In this study, we used transcriptome profiles to investigate the coexpression patterns of gene networks associated with sugar and organic acid metabolism. We identified 3 gene networks/modules containing 2443 genes highly correlated with sugars and organic acids. Within these modules, based on intramodular significance and Reverse Transcription Quantitative polymerase chain reaction (RT-qPCR), we identified 7 genes involved in the metabolism of sugars and organic acids. Among these genes, Cla97C01G000640, Cla97C05G087120 and Cla97C01G018840 (r2 = 0.83 with glucose content) were identified as sugar transporters (SWEET, EDR6 and STP) and Cla97C03G064990 (r2= 0.92 with sucrose content) was identified as a sucrose synthase from information available for other crops. Similarly, Cla97C07G128420, Cla97C03G068240 and Cla97C01G008870, having strong correlations with malic (r2 = 0.75) and citric acid (r2 = 0.85), were annotated as malate and citrate transporters (ALMT7, CS, and ICDH). The expression profiles of these 7 genes in diverse watermelon genotypes revealed consistent patterns of expression variation in various types of watermelon. These findings add significantly to our existing knowledge of sugar and organic acid metabolism in watermelon.

Highlights

Watermelon is the fifth most consumed fleshy fruit worldwide, with a global yield of 118 million tons in20171
A significant difference was observed in soluble sugar content, i.e., glucose, sucrose, and fructose, over the course of watermelon fruit development
An increase in the glucose content was observed from 10 DAP to 18 DAP (37.01 and 32.15 mg/g FW), but at 34 DAP, the glucose content was the same as that observed at 10 DAP (13.42 mg/g FW in sweet watermelon (SwtW) and 16.54 mg/g FW in sour watermelon (SrW)) (Fig. 1c)

Summary

Introduction

Watermelon is the fifth most consumed fleshy fruit worldwide, with a global yield of 118 million tons in20171. Fruits of watermelon are rich in water and nutrients (amino acid sugars, carotenoids, lycopene, organic acids, etc.)[2,3]. These phytochemicals make watermelon one of the most nutritious fruits, providing substantial nutritional supplementation to the human diet[4,5,6,7]. Sugars and organic acids have a strong influence on organoleptic fruit quality and are crucial components involved in the development of fruit flavor[8]. Watermelon fruits undergo numerous biochemical changes, including changes in sugar metabolism, organic acid and pigment accumulation, fruit softening, flavor, and aromatic volatile contents[9]

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Discussion

Conclusion