Abstract

Organic acids and soluble sugars are the major determinants of fruit organoleptic quality. Additionally, DNA methylation has crucial regulatory effects on various processes. However, the epigenetic modifications in the regulation of organic acid and soluble sugar accumulation in apple fruits remain uncharacterized. In this study, DNA methylation and the transcriptome were compared between ‘Honeycrisp’ and ‘Qinguan’ mature fruits, which differ significantly regarding soluble sugar and organic acid contents. In both ‘Honeycrisp’ and ‘Qinguan’ mature fruits, the CG context had the highest level of DNA methylation, and then CHG and CHH contexts. The number and distribution of differentially methylated regions (DMRs) varied among genic regions and transposable elements. The DNA methylation levels in all three contexts in the DMRs were significantly higher in ‘Honeycrisp’ mature fruits than in ‘Qinguan’ mature fruits. A combined methylation and transcriptome analysis revealed a negative correlation between methylation levels and gene expression in DMRs in promoters and gene bodies in the CG and CHG contexts and in gene bodies in the CHH context. Two candidate genes (MdTSTa and MdMa11), which encode tonoplast-localized proteins, potentially associated with fruit soluble sugar contents and acidity were identified based on expression and DNA methylation levels. Overexpression of MdTSTa in tomato increased the fruit soluble sugar content. Moreover, transient expression of MdMa11 in tobacco leaves significantly decreased the pH value. Our results reflect the diversity in epigenetic modifications influencing gene expression and will facilitate further elucidating the complex mechanism underlying fruit soluble sugar and organic acid accumulation.

Highlights

  • Because soluble sugars are mainly stored in vacuoles, we focused on identifying candidate genes encoding tonoplast-localized proteins that are expressed in both ‘HC’ and

  • Apple is an important fruit crop which widely cultivated in temperate regions worldwide

  • Apple fruits are very popular among consumers because of their high organoleptic quality, which is mainly influenced by soluble sugars and organic acids [1,2,41]

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Summary

Introduction

Fruit taste is influenced by the content of organic acids, soluble sugars, and volatile compounds, which affects the overall fruit organoleptic quality [1,2]. The concentration of soluble sugars and organic acids in ripening fruits depend on the balance between biosynthesis, degradation, and vacuolar storage. Different sugars, such as sucrose, fructose, and glucose, impart significantly different sweetness [3,4]. The type, content, and relative proportion of organic acids and soluble sugars in mature fruits determine the taste of the fruit. Optimization of the organic acids and soluble

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