Comparative Transcriptome Analysis of the Accumulation of Anthocyanins Revealed the Underlying Metabolic and Molecular Mechanisms of Purple Pod Coloration in Okra (Abelmoschus esculentus L.).

Yanjie Zhang,Fang Cheng,Qing Zhao,Tianjiao Zhang,Huihui Gu,Jianwei Tian,Qiyan Chen,Yan Li,Jinyong Huang,Xiaodong Xie

doi:10.3390/foods10092180

Yanjie Zhang, Fang Cheng + Show 8 more

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https://doi.org/10.3390/foods10092180

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Abstract

Color is an essential agronomic trait and the consumption of high anthocyanin containing vegetables in daily diet does provide benefits to human health, but the mechanisms on anthocyanin accumulation in tender pods of okra (Abelmoschus esculentus L.) were totally unknown. In this study, a wide characterization and quantitation of anthocyanins and flavonols in tender pods of 15 okra varieties were performed by UHPLC-Q-Orbitrap HRMS for the first time. Two major anthocyanins (delphinidin 3-O-sambubioside and cyanidin 3-O-sambubioside) and six kinds of flavonol glycosides (most are quercetin-based) were identified and quantified. The coloration of the purple okra pod mainly arises from the accumulation of both delphinidin 3-O-sambubioside and cyanidin 3-O-sambubioside in most of purple varieties (Hong Yu, Bowling Red and Burgundy), except Jing Orange. The significant differences in the compositions and contents of anthocyanins are responsible for the pod color ranging from brick-red to purplish-red among the various okra cultivars. Furthermore, four representative okra cultivars exhibiting obvious differences in anthocyanin accumulation were further analyzed with transcriptome and more than 4000 conserved differentially expressed genes were identified across the three compared groups (B vs. BR, B vs. HY and B vs. JO). Based on the comprehensive analysis of transcriptomic data, it was indicated that MBW complex consisting of AeMYB114, AeTT8, and AeTTG1 and other transcriptional factors coordinately regulate the accumulation of anthocyanins via the transcriptional regulation of structural genes. Moreover, four independent working models explaining the diversities of anthocyanin pigmentation in okra pods were also proposed. Altogether, these results improved our understanding on anthocyanin accumulation in okra pods, and provided strong supports for the development of okra pod as a functional food in the future.

Highlights

Introduction distributed under the terms andAs natural water-soluble pigments, anthocyanins are widely distributed in land plants and generate the characteristic red, purple, and blue colors in plant tissues and organs, including the leaves, stems, roots, flowers, seeds, and fruits [1]
Through the UHPLC analysis of the total flavonoids extracted from the pod skins of the 15 okra cultivars with a detection wavelength at 535 nm, two major chromatogram peaks of potential anthocyanins were detected in pod skins of Hong Yu, Bowling Red and Burgundy, while only one major peak was found in pod skins of Jing Orange (Figure 1B)
We found that the coloration of the purple okra pod mainly arises from the accumulation of both cyanidin-based and delphinidin-based anthocyanins in most of varieties (Hong Yu, Bowling Red, and Burgundy), except for Jing Orange

Summary

Introduction

As natural water-soluble pigments, anthocyanins are widely distributed in land plants and generate the characteristic red, purple, and blue colors in plant tissues and organs, including the leaves, stems, roots, flowers, seeds, and fruits [1]. The anthocyanin biosynthetic pathway which derives from flavonoid pathway has been extensively studied in Arabidopsis (Arabidopsis thaliana), grape (Vitis vinifera), petunia (Petunia hybrida), snapdragon (Antirrhinum majus), maize (Zea mays), blood orange (Citrussinensis Osbeck L.), and tomato (Solanum lycopersicum) [5,11,12,13]. The structural genes in the flavonoid pathway are highly conserved in plants. Flavonoid biosynthesis begins with the cleavage of phenylalanine catalyzed by phenylalanine ammonia-lyase (PAL), resulting in the generation of cinnamic acid. Dihydrokaempferol is produced from cinnamic acid by a series of enzymes including cinnamate 4-hydroxylase (C4H), 4-coumaroyl: CoA-ligase (4CL), chalcone synthase (CHS), chalcone isomerase (CHI), and flavanone 3-hydroxylase (F3H). The dihydrokaempferol can be further converted to dihydroquercetin and dihydromyricetin by flavanone 30 -hydroxylase (F30 H) and flavanone

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