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

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.

SUBMITTER: Sun B

PROVIDER: S-EPMC7527512 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:MYB transcription factor (TF) is one of the largest TF families and regulates defense responses to various stresses, hormone signaling as well as many metabolic and developmental processes in plants. Understanding these regulatory hierarchies of gene expression networks in response to developmental and environmental cues is a major challenge due to the complex interactions between the genetic elements. Correlation analyses are useful to unravel co-regulated gene pairs governing biological process as well as identification of new candidate hub genes in response to these complex processes. High throughput expression profiling data are highly useful for construction of co-expression networks. In the present study, we utilized transcriptome data for comprehensive regulatory network studies of MYB TFs by "top-down" and "guide-gene" approaches. More than 50% of OsMYBs were strongly correlated under 50 experimental conditions with 51 hub genes via "top-down" approach. Further, clusters were identified using Markov Clustering (MCL). To maximize the clustering performance, parameter evaluation of the MCL inflation score (I) was performed in terms of enriched GO categories by measuring F-score. Comparison of co-expressed cluster and clads analyzed from phylogenetic analysis signifies their evolutionarily conserved co-regulatory role. We utilized compendium of known interaction and biological role with Gene Ontology enrichment analysis to hypothesize function of coexpressed OsMYBs. In the other part, the transcriptional regulatory network analysis by "guide-gene" approach revealed 40 putative targets of 26 OsMYB TF hubs with high correlation value utilizing 815 microarray data. The putative targets with MYB-binding cis-elements enrichment in their promoter region, functional co-occurrence as well as nuclear localization supports our finding. Specially, enrichment of MYB binding regions involved in drought-inducibility implying their regulatory role in drought response in rice. Thus, the co-regulatory network analysis facilitated the identification of complex OsMYB regulatory networks, and candidate target regulon genes of selected guide MYB genes. The results contribute to the candidate gene screening, and experimentally testable hypotheses for potential regulatory MYB TFs, and their targets under stress conditions.

Project description:Perillafrutescen is used as traditional food and medicine in East Asia. Its seeds contain high levels of ?-linolenic acid (ALA), which is important for health, but is scarce in our daily meals. Previous reports on RNA-seq of perilla seed had identified fatty acid (FA) and triacylglycerol (TAG) synthesis genes, but the underlying mechanism of ALA biosynthesis and its regulation still need to be further explored. So we conducted Illumina RNA-sequencing in seven temporal developmental stages of perilla seeds. Sequencing generated a total of 127 million clean reads, containing 15.88 Gb of valid data. The de novo assembly of sequence reads yielded 64,156 unigenes with an average length of 777 bp. A total of 39,760 unigenes were annotated and 11,693 unigenes were found to be differentially expressed in all samples. According to Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, 486 unigenes were annotated in the "lipid metabolism" pathway. Of these, 150 unigenes were found to be involved in fatty acid (FA) biosynthesis and triacylglycerol (TAG) assembly in perilla seeds. A coexpression analysis showed that a total of 104 genes were highly coexpressed (r > 0.95). The coexpression network could be divided into two main subnetworks showing over expression in the medium or earlier and late phases, respectively. In order to identify the putative regulatory genes, a transcription factor (TF) analysis was performed. This led to the identification of 45 gene families, mainly including the AP2-EREBP, bHLH, MYB, and NAC families, etc. After coexpression analysis of TFs with highly expression of FAD2 and FAD3 genes, 162 TFs were found to be significantly associated with two FAD genes (r > 0.95). Those TFs were predicted to be the key regulatory factors in ALA biosynthesis in perilla seed. The qRT-PCR analysis also verified the relevance of expression pattern between two FAD genes and partial candidate TFs. Although it has been reported that some TFs are involved in seed development, more direct evidence is still needed to verify their function. However, these findings can provide clues to reveal the possible molecular mechanisms of ALA biosynthesis and its regulation in perilla seed.

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

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