Coexpression network analysis reveals an MYB transcriptional activator involved in capsaicinoid biosynthesis in hot peppers

Binmei Sun,Muxi Chen,Zhangsheng Zhu,Fanrong Cao,Shaoqun Liu,Bihao Cao,Jianjun Lei,Kunhao Chen,Xin Zhou,Changming Chen,Guoju Chen,Chengjie Chen

doi:10.1038/s41438-020-00381-2

Abstract

Plant biosynthesis involves numerous specialized metabolites with diverse chemical natures and biological activities. The biosynthesis of metabolites often exclusively occurs in response to tissue-specific combinatorial developmental cues that are controlled at the transcriptional level. Capsaicinoids are a group of specialized metabolites that confer a pungent flavor to pepper fruits. Capsaicinoid biosynthesis occurs in the fruit placenta and combines its developmental cues. Although the capsaicinoid biosynthetic pathway has been largely characterized, the regulatory mechanisms that control capsaicinoid metabolism have not been fully elucidated. In this study, we combined fruit placenta transcriptome data with weighted gene coexpression network analysis (WGCNA) to generate coexpression networks. A capsaicinoid-related gene module was identified in which the MYB transcription factor CaMYB48 plays a critical role in regulating capsaicinoid in pepper. Capsaicinoid biosynthetic gene (CBG) and CaMYB48 expression primarily occurs in the placenta and is consistent with capsaicinoid biosynthesis. CaMYB48 encodes a nucleus-localized protein that primarily functions as a transcriptional activator through its C-terminal activation motif. CaMYB48 regulates capsaicinoid biosynthesis by directly regulating the expression of CBGs, including AT3a and KasIa. Taken together, the results of this study indicate ways to generate robust networks optimized for the mining of CBG-related regulators, establishing a foundation for future research elucidating capsaicinoid regulation.

Highlights

Hot pepper (Capsicum spp.) is the most popular vegetable and ingredient in the world because of its attractive spicy flavor[1,2]
These results suggested that CaMYB48 might regulate the coexpressed Capsaicinoid biosynthetic gene (CBG) to regulate capsaicinoid biosynthesis
The results revealed a high abundance of CaMYB48 detected in the placenta from 16 days post-anthesis (DPA) to 33 DPA, and the key CBGs AMT, KasIa, and AT3a were highly expressed at these stages (Fig. 3c), implying that CaMYB48 might govern the expression of these genes

Summary

Introduction

Hot pepper (Capsicum spp.) is the most popular vegetable and ingredient in the world because of its attractive spicy flavor[1,2]. The capsaicinoid biosynthesis process is strictly switched spatially and temporally, and the expression of CBGs in pepper is precisely regulated at the transcriptional level[4,21]. The expression level of a major transcription factor usually affects the transcript level of all genes in the biosynthetic pathway, which will change the accumulation of compounds[5,22,23]. Catharanthus roseus ORCA3 is a crucial transcription factor that regulates the expression of terpenoid indole alkaloid genes, and overexpression of ORCA3 results in 3.2-fold-increased accumulation of terpenoid indole alkaloids[24]. In horticultural plants, such as tomato (Solanum lycopersicum)[25], tea (Camellia sinensis)[26], and orange (Citrus sinensis)[27], high accumulation of health-promoting anthocyanins, which arise from upregulation of the anthocyanin-related MYB transcriptional activator, leads to anthocyanin biosynthetic gene expression simultaneously. The identification of capsaicinoid biosynthesis-related transcription factors is needed

Methods

Results

Conclusion