How Does Nature Create the Painting “Gradient Coloration of ‘Manicure Finger’ Grape”? Integrated Omics Unveil the Pigments Basis and Metabolism Networks of Its Formation

ABSTRACT ‘Manicure Finger’ grape exhibits gradient coloration during veraison, where the lower part of the skin changes color faster and intenser than the upper, giving the same berry a gradient color from green on the top to red on the bottom. This unique characteristic distinguishes it from other table grape varieties and makes it highly commercially valuable. However, because the formation mechanisms of gradient coloration are unclear, ‘Manicure Finger’ lags behind other grapes in the development of breeding, cultivation, and storage technologies, occupying only a small share of the table grape market. Here, based on integrated omics including anthocyanin, flavonoid metabolome, and transcriptome, the substances basis and metabolic mechanisms regulating gradient coloration were thoroughly resolved. In ‘Manicure Finger’, eight anthocyanins including malvidin‐3‐ O ‐glucoside, peonidin‐3‐ O ‐glucoside, and cyanidin‐3‐ O ‐glucoside were identified as color‐presenting substances, while flavones and flavonols, especially kaempferol‐3‐ O ‐rutinoside and quercetin‐3‐ O ‐glucoside, functioned as co‐pigments. Spatial differences in their accumulation were substances basis for gradient coloration. In the lower skin, these substances accumulated faster due to the higher expression levels of structural genes VvF3 ´ 5 ´ H1 , VvF3 ´ 5 ´ H2 , VvANS , VvGT1 , and VvFAOMT , which were further modulated by transcription factors VvMYBA1 , VvMYBA2 , VvMYBA3 , and VvMYBA6 . Novel transcription factors VvbHLH148 , VvMYBA22 , and VvMYBA3 were also most probably involved in this regulatory process. Histone acylation regulated by VvHAC1 and lysine methylation regulated by VvHMT1 might underlie the epigenetic basis of gradient coloration. Overall, the metabolic networks underlying gradient coloration were comprehensively constructed at levels of color‐presenting substances, structural genes and transcription factors, offering valuable insights into the precise regulation of ‘Manicure Finger’ color formation.