Integration of morphological, physiological and multi-omics analysis reveals a comprehensive mechanism for cuticular wax during development of greasiness in postharvest apples.

Skin greasiness is a common postharvest disorder of apple (Malus × domestica). However, the molecular mechanism of skin greasiness is unclear. In this study, fruits of 'Golden Delicious' (GD), 'Granny Smith', and 'Fuji' with distinct characteristics of greasiness were used for greasiness scoring, wax morphology, wax metabolite, and RNA-seq analyses. Additionally, GD fruit were treated with 1-methylcyclopropene (1-MCP), which repressed greasiness. A partial least squares discriminant analysis (PLS-DA) revealed that wax esters were the critical wax fraction for skin greasiness. Among these wax esters, liquid linoleate esters of short-chain alcohols (C4-C6) and farnesol showed increased contents with increasing greasiness. Their concentrations were significantly correlated with greasiness score. To identify the genes encoding key enzymes for the synthesis of liquid linoleate esters, a weighted gene co-expression network analysis was conducted. MdDCR1, encoding an acyltransferase (defective in cuticular ridges, DCR), was selected as a candidate gene. MdDCR1 was significantly upregulated in greasy skin, and significantly suppressed by 1-MCP treatment. MdDCR1 silencing suppressed the accumulation of liquid linoleate esters of short-chain alcohols, including butyl linoleate, pentyl linoleate, and hexyl linoleate, in GD skin. These results provide insights into the molecular mechanisms of cuticular wax metabolism related to skin greasiness in apple. Our results show that transcriptional regulation of MdDCR1, encoding an acyltransferase that catalyzes the biosynthesis of liquid linoleate esters of short-chain alcohols (C4-C6) via an independent side branch of the C18:2 CoA pathway, regulates the formation of greasiness.