Light dependent anthocyanin accumulation contributes to the red pigmentation of the fruit skin of mango (Mangifera indica L.). Light-independent pigmentation has also been reported, but remains poorly characterized. In this study, the pigmentation patterns in the skin of two red mango cultivars, ‘Ruby’ and ‘Sensation’, were evaluated. Metabolomic profiling revealed that quercetin-3-O-glucoside, cyanidin-3-O-galactoside, procyanidin B1, and procyanidin B3 are the predominant flavonoid compounds in the skin of ‘Ruby’ and ‘Sensation’ fruit. Young fruit skin mainly accumulates flavonol and proanthocyanidin, while anthocyanin is mainly accumulated in the skin of mature fruit. Bagging treatment inhibited the biosynthesis of flovonol and anthocyanin, but promoted the accumulation of proanthocyanidin. Compared with ‘Sensation’, matured ‘Ruby’ fruit skin showed light red pigmentation at 120 days after full bloom (DAFB), showing a light-independent anthocyanin accumulation pattern. However, the increase of anthocyanin concentration, and the expression of key anthocyanin structural and regulatory genes MiUFGT1, MiUFGT3, and MiMYB1 in the skin of bagged ‘Ruby’ fruit versus ‘Sensation’ at 120 DAFB was very limited. There was no mutation in the crucial elements of MiMYB1 promoter between ‘Ruby’ and ‘Sensation’. We hypothesize that the light-independent anthocyanin accumulation in the skin of mature ‘Ruby’ fruit is regulated by plant hormones, and that ‘Ruby’ can be used for breeding of new more easily pigmented red mango cultivars.

The WRKY family is one of the largest transcription factor (TF) families in plants and is involved in the regulation of plant physiological processes, such as anthocyanin accumulation. However, little information is known regarding the WRKY genes in the mango. In this study, a total of 87 mango WRKY genes were identified and named MiWRKY1 to MiWRKY87. Phylogenetic results showed that the 87 MiWRKYs could be divided into three groups (I, II, III) and five subgroups of group II (II-a, II-b, II-c, II-d, II-e), with high similarity in exon–intron structures and WRKY domain and motif compositions within the same group and subgroup. One tandem duplication (MiWRKY76 and MiWRKY82) and 97 pairs of segmental duplicates were identified in the mango genome. Syntenic analysis showed that mango MiWRKY genes had 52 and 69 orthologous pairs with Arabidopsis and citrus, respectively. Promoter cis-acting element analysis revealed that MiWRKYs contain a large number of elements associated with light signaling, hormonal response, environmental stress, and plant development. Tissue specific expression profiles showed that the expression of MiWRKY genes displayed tissue preference. Quantitative-PCR analysis showed that high expression levels of MiWRKY1, MiWRKY3, MiWRKY5, MiWRKY81, and MiWRKY84 were detected in the skin of red mango cultivar, and the expressions of MiWRKY1 and MiWRKY81 were up-regulated during light-induced anthocyanin accumulation in the mango, indicating these genes might regulate anthocyanin biosynthesis in the mango. This study provides comprehensive genetic information on the MiWRKYs in mango fruit.

Light is one the most important environmental factors regulating the accumulation of specific metabolites in plants, such as flavonoid. Chalcone synthase (CHS) is the key rate-limiting enzyme of the flavonoid biosynthesis pathway, while little is known about the CHS genes in mango (Mangifera indica L.). Therefore, the aim of the study was to obtain the genome-wide identification of the CHS genes in mango and screen the light-responsive family members. In this study, a total of 21 CHS genes were identified from the mango genome, and most of the members contained the Cys-His-Asn triad and the CHS/STS signature motif. Most of the MiCHS genes were located on chromosomes 2 and 4, and seven pairs of tandem duplication genes and five pairs of segmental duplication genes were detected among the MiCHS members. The expression of MiCHSs showed a tissue-specific pattern and was not correlated with the flavonoid or anthocyanin accumulation in cultivars with different peel colors. MiCHS4, MiCHS16 and MiCHS17 were found to respond to preharvest and postharvest UV-B plus visible light treatments, which exhibited no significant relationship with the light-responsive cis-acting element distribution in the promoter region. Our results are helpful and can be used to further study the function of MiCHS genes in light-induced flavonoid biosynthesis in mango.

The biosynthesis of anthocyanins and proanthocyanidins (PAs), components of two main flavonoids in plants, is regulated by environmental factors such as light. We previously found that bagging significantly repressed the biosynthesis of anthocyanins in red ‘Ruby’ mango fruit peel, but induced the accumulation of PAs. However, the molecular mechanism remains unclear. In the current study, transcriptome sequencing was used for screening the essential genes responsible for the opposite accumulation pattern of anthocyanins and PAs by bagging treatment. According to weighted gene co-expression network analysis (WGCNA), structural genes and transcription factors highly positively correlated to anthocyanins and PAs were identified. One flavanone 3-hydroxylase (F3H) and seven structural genes, including one chalcone synthase (CHS), one flavonoid 3’-hydroxylase (F3’H), one anthocyanidin synthesis (ANS), three leucoanthocyanidin reductase (LARs), and one UDP glucose: flavonoid 3-O-glucosyltransferase (UFGT), are crucial for anthocyanin and PA biosynthesis, respectively. In addition to MYB and bHLH, ERF, C2H2, HD-ZIP, and NAC are important transcription factors that participate in the regulation of anthocyanin and PA biosynthesis in ‘Ruby’ mango fruit peel by bagging treatment. Our results are helpful for revealing the transcription regulation mechanism of light-regulated mango anthocyanin and PA biosynthesis, developing new technologies for inducing flavonoid biosynthesis in mangos, and breeding mango cultivars containing high concentrations of flavonoids.