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Genome-Wide Identification of R2R3-MYB Transcription Factors: Discovery of a "Dual-Function" Regulator of Gypenoside and Flavonol Biosynthesis in Gynostemma pentaphyllum.

ABSTRACT: The R2R3-MYB gene family participates in several plant physiological processes, especially the regulation of the biosynthesis of secondary metabolites. However, little is known about the functions of R2R3-MYB genes in Gynostemma pentaphyllum (G. pentaphyllum), a traditional Chinese medicinal herb that is an excellent source of gypenosides (a class of triterpenoid saponins) and flavonoids. In this study, a systematic genome-wide analysis of the R2R3-MYB gene family was performed using the recently sequenced G. pentaphyllum genome. In total, 87 R2R3-GpMYB genes were identified and subsequently divided into 32 subgroups based on phylogenetic analysis. The analysis was based on conserved exon-intron structures and motif compositions within the same subgroup. Collinearity analysis demonstrated that segmental duplication events were majorly responsible for the expansion of the R2R3-GpMYB gene family, and Ka/Ks analysis indicated that the majority of the duplicated R2R3-GpMYB genes underwent purifying selection. A combination of transcriptome analysis and quantitative reverse transcriptase-PCR (qRT-PCR) confirmed that Gynostemma pentaphyllum myeloblastosis 81 (GpMYB81) along with genes encoding gypenoside and flavonol biosynthetic enzymes exhibited similar expression patterns in different tissues and responses to methyl jasmonate (MeJA). Moreover, GpMYB81 could bind to the promoters of Gynostemma pentaphyllum farnesyl pyrophosphate synthase 1 (GpFPS1) and Gynostemma pentaphyllum chalcone synthase (GpCHS), the key structural genes of gypenoside and flavonol biosynthesis, respectively, and activate their expression. Altogether, this study highlights a novel transcriptional regulatory mechanism that suggests that GpMYB81 acts as a "dual-function" regulator of gypenoside and flavonol biosynthesis in G. pentaphyllum.

SUBMITTER: Huang D

PROVIDER: S-EPMC8767017 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGypenosides are a group of triterpene saponins from Gynostemma pentaphyllum that are the same as or very similar to ginsenosides from the Panax species. Several enzymes involved in ginsenoside biosynthesis have been characterized, which provide important clues for elucidating the gypenoside biosynthetic pathway. We suppose that gypenosides and ginsenosides may have a similar biosynthetic mechanism and that the corresponding enzymes in the two pathways may have considerable similarity in their sequences. To further understand gypenoside biosynthesis, we sequenced the G. pentaphyllum transcriptome with a hybrid sequencing-based strategy and then determined the candidate genes involved in this pathway using phylogenetic tree construction and gene expression analysis.ResultsFollowing the PacBio standard analysis pipeline, 66,046 polished consensus sequences were obtained, while Illumina data were assembled into 140,601 unigenes with Trinity software. Then, these output sequences from the two analytical routes were merged. After removing redundant data with CD-HIT software, a total of 140,157 final unigenes were obtained. After functional annotation, five 2,3-oxidosqualene cyclase genes, 145 cytochrome P450 genes and 254 UDP-glycosyltransferase genes were selected for the screening of genes involved in gypenoside biosynthesis. Using phylogenetic analysis, several genes were divided into the same subfamilies or closely related evolutionary branches with characterized enzymes involved in ginsenoside biosynthesis. Using real-time PCR technology, their expression patterns were investigated in different tissues and at different times after methyl jasmonate induction. Since the genes in the same biosynthetic pathway are generally coexpressed, we speculated that GpOSC1, GpCYP89, and GpUGT35 were the leading candidates for gypenoside biosynthesis. In addition, six GpWRKYs and one GpbHLH might play a possible role in regulating gypenoside biosynthesis.ConclusionsWe developed a hybrid sequencing strategy to obtain longer length transcriptomes with increased accuracy, which will greatly contribute to downstream gene screening and characterization, thus improving our ability to elucidate secondary metabolite biosynthetic pathways. With this strategy, we found several candidate genes that may be involved in gypenoside biosynthesis, which laid an important foundation for the elucidation of this biosynthetic pathway, thus greatly contributing to further research in metabolic regulation, synthetic biology and molecular breeding in this species.

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Genome-Wide Identification of R2R3-MYB Transcription Factors: Discovery of a "Dual-Function" Regulator of Gypenoside and Flavonol Biosynthesis in Gynostemma pentaphyllum.

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