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Metabolomics integrated with transcriptomics reveals the distribution of iridoid and crocin metabolic flux in Gardenia jasminoides Ellis.

ABSTRACT: Gardenia jasminoides Ellis (G. jasminoides) fruits are used as a resource for obtaining natural colorants and in traditional Chinese herbal medicine. However, G. jasminoides presents a relatively long flowering period and different ripening periods, so there are significant differences in the accumulation of metabolites in fruits of different colors. In addition, the complete metabolic pathways of iridoidsand crocins, which are used as medicinal composition of G. jasminoides, are poorly understood at present. In this research, we comprehensively compared the transcriptome and metabolites profiles of the developmental stages and locations of iridoid and crocin biosynthesis. A large number of differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) were detected in four groups of samples, and clear variation in the pattern of metabolite abundance and gene expression were observed among different fruit colors and parts. Geniposide and gardenoside mainly accumulated in the sarcocarp of green fruit (GFS) and the sarcocarp of red fruit (FS), respectively. Crocin mainly accumulated in the peel and sarcocarp of red fruits. In the iridoid pathway, we hypothesized that there was a transport mechanism from the sarcocarp to the peel of G. jasminoides because of the inconsistent expression of G8O, 10-HGO and IS associated with differences in fruit ripening. UGTs play an important role in the biosynthesis of the active components of G. jasminoides. Combined transcriptome and metabonomics analysis showed a negative correlation between the biosynthesis of geniposide and crocin. The redirection of the metabolic flux and the regulation of key enzymes may be the main reasons for the changes in the biosynthesis of iridoid and crocin in G. jasminoides fruit. Our study expended valuable information for functional genomic library and provided new insights for metabolic engineering of secondary metabolite in G. Jasminoides.

SUBMITTER: Pan Y

PROVIDER: S-EPMC8432746 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The petal senescence of ethylene insensitive species has not been investigated thoroughly while little is known about the temporal and tissue specific expression patterns of transcription factors (TFs) in this developmental process. Even less is known on flower senescence of the ornamental pot plant Gardenia jasminoides, a non climacteric flower with significant commercial value. RESULTS: We initiated a de novo transcriptome study to investigate the petal senescence in four developmental stages of cut gardenia flowers considering that the visible symptoms of senescence appear within 4 days of flower opening. De novo assembly of transcriptome sequencing resulted in 102,263 contigs with mean length of 360 nucleotides that generated 57,503 unigenes. These were further clustered into 20,970 clusters and 36,533 singletons. The comparison of the consecutive developmental stages resulted in 180 common, differentially expressed unigenes. A large number of Simple Sequence Repeats were also identified comprising a large number of dinucleotides and trinucleotides. The prevailing families of differentially expressed TFs comprise the AP2/EREBP, WRKY and the bHLH. There are 81 differentially expressed TFs when the symptoms of flower senescence become visible with the most prevailing being the WRKY family with 19 unigenes. No other WRKY TFs had been identified up to now in petal senescence of ethylene insensitive species. A large number of differentially expressed genes were identified at the initiation of visible symptoms of senescence compared to the open flower stage indicating a significant shift in the expression profiles which might be coordinated by up-regulated and/or down-regulated TFs. The expression of 16 genes that belong to the TF families of WRKY, bHLH and the ethylene sensing pathway was validated using qRT--PCR. CONCLUSION: This de novo transcriptome analysis resulted in the identification of TFs with specific temporal expression patterns such as two WRKYs and one bHLH, which might play the role of senescence progression regulators. Further research is required to investigate their role in gardenia flowers in order to develop tools to delay petal senescence.

Project description:Estrogen-stimulating principles have been demonstrated to relieve postmenopausal syndrome effectively. Gardenia jasminoides Ellis (GJE) is an herbal medicine possessing multiple pharmacological effects on human health with low toxicity. However, the therapeutic effects of GJE on the management of postmenopausal syndrome and its mechanism of action have not been fully elucidated. In this study, network pharmacology-based approaches were employed to examine steroidogenesis under the influence of GJE. In addition, the possibility of toxicity of GJE was ruled out and four probable active compounds were predicted. In parallel, a chromatographic fraction of GJE with estrogen-stimulating effect was identified and nine major compounds were isolated from this active fraction. Among the nine compounds, four of them were identified by network pharmacology, validating the use of network pharmacology to predict active compounds. Then the phenotypic approaches were utilized to verify that rutin, chlorogenic acid (CGA) and geniposidic acid (GA) exerted an estrogen-stimulating effect on ovarian granulosa cells. Furthermore, the results of target-based approaches indicated that rutin, CGA, and GA could up-regulate the FSHR-aromatase pathway in ovarian granulosa cells. The stimulation of estrogen production by rat ovarian granulosa cells under the influence of the three compounds underwent a decline when the follicle-stimulating hormone receptor (FSHR) was blocked by antibodies against the receptor, indicating the involvement of FSHR in the estradiol-stimulating activity of the three compounds. The effects of the three compounds on estrogen biosynthesis- related gene expression level were further confirmed by Western blot assay. Importantly, the MTT results showed that exposure of breast cancer cells to the three compounds resulted in reduction of cell viability, demonstrating the cytotoxicity of the three compounds. Collectively, rutin, chlorogenic acid and geniposidic acid may contribute to the therapeutic potential of GJE for the treatment of postmenopausal syndrome.

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Metabolomics integrated with transcriptomics reveals the distribution of iridoid and crocin metabolic flux in Gardenia jasminoides Ellis.

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