Summary Plants produce countless specialized metabolites crucial for their development and fitness, and many are useful bioactive compounds. Capsaicinoids are intriguing genus‐specialized metabolites that confer a pungent flavor to Capsicum fruits, and they are widely applied in different areas. Among the five domesticated Capsicum species, Capsicum chinense has a high content of capsaicinoids, which results in an extremely hot flavor. However, the species‐specific upregulation of capsaicinoid‐biosynthetic genes (CBGs) and the evolution of extremely pungent peppers are not well understood. We conducted genetic and functional analyses demonstrating that the quantitative trait locus Capsaicinoid1 (Cap1), which is identical to Pun3 contributes to the level of pungency. The Cap1/Pun3 locus encodes the Solanaceae‐specific MYB transcription factor MYB31. Capsicum species have evolved placenta‐specific expression of MYB31, which directly activates expression of CBGs and results in genus‐specialized metabolite production. The capsaicinoid content depends on MYB31 expression. Natural variations in the MYB31 promoter increase MYB31 expression in C. chinense via the binding of the placenta‐specific expression of transcriptional activator WRKY9 and augmentation of CBG expression, which promotes capsaicinoid biosynthesis. Our findings provide insights into the evolution of extremely pungent C. chinense, which is due to natural variations in the master regulator, and offers targets for engineering or selecting flavor in Capsicum.
Petal senescence is a complex programmed process. It has been demonstrated previously that treatment with ethylene, a plant hormone involved in senescence, can extensively alter transcriptome and proteome profiles in plants. However, little is known regarding the impact of ethylene on posttranslational modification (PTM) or the association between PTM and the proteome. Protein degradation is one of the hallmarks of senescence, and ubiquitination, a major PTM in eukaryotes, plays important roles in protein degradation. In this study, we first obtained reference petunia (Petunia hybrida) transcriptome data via RNA sequencing. Next, we quantitatively investigated the petunia proteome and ubiquitylome and the association between them in petunia corollas following ethylene treatment. In total, 51,799 unigenes, 3,606 proteins, and 2,270 ubiquitination sites were quantified 16 h after ethylene treatment. Treatment with ethylene resulted in 14,448 down-regulated and 6,303 up-regulated unigenes (absolute log fold change > 1 and false discovery rate < 0.001), 284 down-regulated and 233 up-regulated proteins, and 320 up-regulated and 127 down-regulated ubiquitination sites using a 1.5-fold threshold (P < 0.05), indicating that global ubiquitination levels increase during ethylene-mediated corolla senescence in petunia. Several putative ubiquitin ligases were up-regulated at the protein and transcription levels. Our results showed that the global proteome and ubiquitylome were negatively correlated and that ubiquitination could be involved in the degradation of proteins during ethylene-mediated corolla senescence in petunia. Ethylene regulates hormone signaling transduction pathways at both the protein and ubiquitination levels in petunia corollas. In addition, our results revealed that ethylene increases the ubiquitination levels of proteins involved in endoplasmic reticulum-associated degradation.
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.
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