The Biases in Flavonoids and Anthocyanin Biosynthesis of a Red Flesh Table Grape Revealed by Metabolome and Transcriptome Co-analysis

Abstract

Red flesh is a welcomed fruit trait, yet the regulation of red flesh formation in grape is not well understood. ‘Mio Red’ is a seedless table grape variety with light red flesh and blue-purple skin, the flesh color developed in the late stage of berry ripening, remarkably later than the skin coloring at veraison. The flesh and skin flavonoids metabolome and the transcriptome were analyzed. A total of 173 flavonoids including 17 anthocyanins were identified, 68 were found significantly different (Fold change ≥ 2 or ≤ 0. 5, VIP ≥ 1). Quercetin 3-O-glucoside, epicatechin-epiafzelechin, apigenin 6,8-C-diglucoside and hesperetin 5-O-glucoside were of higher content in the flesh, while the rest flavonoids were of higher content in the skin. The main anthocyanin in the flesh was pelargonidin derivatives in contrast to peonidin derivatives in the skin. Transcriptome comparison recruited 3970 differentially expressed genes (DEGs, log2Fold change > = 1, FDR < 0.05, FPKM ≥ 1), among them 57 were structural genes of flavonoid metabolism pathway. Two anthocyanin synthase (ANS) DEGs were annotated, ANS1 (Vitvi11g00565) and ANS2 (Vitvi02g00435) led the expression in the flesh and skin respectively. In the flesh, anthocyanin biosynthesis structural gene UFGT, positive regulators MYBA1/2/3, and anthocyanin transporters GST14 and MATE5 were of significantly lower expression, while negative regulators MYBC2-L1 and MYB3 were of higher transcription. The results of this study provide new information in the coloring mechanism of red flesh grape and assisting breeding of future table grapes having higher content of phytonutrient providing the health benefit as red wines.

Anthocyanin physiology and biochemistry in fleshy fruit species: Mangosteen as a model

“…These values, however, depended on the cultivar and maturity stage. The major anthocyanins found in the mangosteen pericarp were cyanidin‐3‐sophoroside and cyanidin‐3‐glucoside (Jamil et al., 2023; Palapol, Ketsa, Stevenson, et al., 2009), while the main anthocyanin(s) identified in red apple was cyanidin‐3‐ O ‐galactoside (Y. Liu et al., 2013; Shi et al., 2022), in Malay apple was cyanidin‐3‐ O ‐glucoside (Kotepong et al., 2019), in blueberry was malvidin‐3‐galactoside (S. Wang, Wang, et al., 2022), in sweet cherry was cyanidin‐3‐rutinoside with cyanidin‐3‐glucoside being the second most prominent (Chaovanalikit & Wrostad, 2004), in both plum (Usenik et al., 2009) and litchi was cyanidin‐3‐rutinoside (He et al., 2022; Rivera‐López et al., 1999; Z. Zhang et al., 2004), in red pomegranate were cyanidin‐3,5‐diglucoside and cyanidin‐3‐glucoside (Zhao et al., 2015), in table grape were cyanidin‐3,5‐ O ‐diglucoside and cyanidin‐3‐ O ‐glucoside (Kőrösi et al., 2022; Lu et al., 2023), in muscadine grape was delphinidin‐3,5‐diglucoside (Yuzuak & Xie, 2022), in rambutan was cyanidin‐3‐ O ‐glucoside (Monrroy et al., 2020), in red raspberry was cyanidin‐3‐ O ‐sophoroside (Teng et al., 2017), and in strawberry was pelargonidin‐3‐ O ‐glucoside (Cho et al., 2021; da Silva et al., 2007; Dzhanfezova et al., 2020; Karaaslan & Yaman, 2017; Miao et al., 2016). There were, therefore, considerable differences among these different fruits in the type of glycoside and the type of anthocyanidin that was present.…”

“…The genes that have been identified as being involved in the regulation of the anthocyanin biosynthetic pathway in a number of different fruits consist of many genes that encode the enzymes involved in the synthesis of anthocyanins (Table 1). The high expression of genes shown in Table 1 has been correlated with anthocyanin accumulation in both colored and noncolored fruit, and their skin and flesh, in a range of fruits including apple (Honda et al., 2002; C. Ma et al., 2019; Shi et al., 2022), grape (Boss et al., 1996; Ge et al., 2022; Jeong et al., 2004; Lu et al., 2023), litchi (He et al., 2022; Lai et al., 2014), mango (Bajpai et al., 2018), Malay apple (Kotepong et al., 2011, 2019), peach (Cao et al., 2018; X. Liu et al., 2019; Rahim et al., 2014; Tsuda et al., 2004; Ye et al., 2019), pear (J. Liu, Deng, et al., 2021), and pomegranate (Zhao et al., 2015).…”