Dataset Information

RNA-Seq analysis reveals the important co-expressed genes associated with polyphyllin biosynthesis during the developmental stages of Paris polyphylla.

ABSTRACT:

Background

Plants synthesize metabolites to adapt to a continuously changing environment. Metabolite biosynthesis often occurs in response to the tissue-specific combinatorial developmental cues that are transcriptionally regulated. Polyphyllins are the major bioactive components in Paris species that demonstrate hemostatic, anti-inflammatory and antitumor effects and have considerable market demands. However, the mechanisms underlying polyphyllin biosynthesis and regulation during plant development have not been fully elucidated.

Results

Tissue samples of P. polyphylla var. yunnanensis during the four dominant developmental stages were collected and investigated using high-performance liquid chromatography and RNA sequencing. Polyphyllin concentrations in the different tissues were found to be highly dynamic across developmental stages. Specifically, decreasing trends in polyphyllin concentration were observed in the aerial vegetative tissues, whereas an increasing trend was observed in the rhizomes. Consistent with the aforementioned polyphyllin concentration trends, different patterns of spatiotemporal gene expression in the vegetative tissues were found to be closely related with polyphyllin biosynthesis. Additionally, molecular dissection of the pathway components revealed 137 candidate genes involved in the upstream pathway of polyphyllin backbone biosynthesis. Furthermore, gene co-expression network analysis revealed 74 transcription factor genes and one transporter gene associated with polyphyllin biosynthesis and allocation.

Conclusions

Our findings outline the framework for understanding the biosynthesis and accumulation of polyphyllins during plant development and contribute to future research in elucidating the molecular mechanism underlying polyphyllin regulation and accumulation in P. polyphylla.

SUBMITTER: Gao X

PROVIDER: S-EPMC9354290 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Publications

RNA-Seq analysis reveals the important co-expressed genes associated with polyphyllin biosynthesis during the developmental stages of Paris polyphylla.

Gao Xiaoyang X Su Qixuan Q Li Jing J Yang Wenjing W Yao Baolin B Guo Jiawei J Li Shengying S Liu Changning C

BMC genomics 20220805 Suppl 1

<h4>Background</h4>Plants synthesize metabolites to adapt to a continuously changing environment. Metabolite biosynthesis often occurs in response to the tissue-specific combinatorial developmental cues that are transcriptionally regulated. Polyphyllins are the major bioactive components in Paris species that demonstrate hemostatic, anti-inflammatory and antitumor effects and have considerable market demands. However, the mechanisms underlying polyphyllin biosynthesis and regulation during plant ...[more]

PMID: 35931959

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Project description:IntroductionPolyphyllin from Paris polyphylla var. yunnanensis exhibits anti-inflammatory, analgesic, antibacterial, and antiviral properties. However, the current production of polyphyllin can barely meet market demand. To improve the content of polyphyllin produced by P. polyphylla, two endophyte strains, Bacillus cereus LgD2 and Fusarium oxysporum TPB, were isolated from Paris fargesii Franch. and inoculated in the roots of P. polyphylla. Both symbiotic strains significantly promoted the accumulation of saponins in P. polyphylla.MethodsThe content of polyphyllin in rhizomes of P. polyphylla treated with TPB with LgD2 strain was determined using High Performance Liquid Chromatography and the expressed genes were analyzed by RNA-seq. Gene Ontology and Kyoto Encyclopedia of Genes annotations were performed on the differentially expressed genes, a clustering tree of UDP-glycosyltransferase (UGT) and cytochrome P450 (CYP450) gene families was constructed, and UGT and CYP450 involved in the biosynthesis of polyphyllin were predicted using weighted correlation network analysis (WGCNA).ResultsRNA-seq and qRT-PCR analyses showed that endophytic inoculation did not promote polyphyllin accumulation by enhancing the upstream terpene biosynthesis pathway, but probably by up-regulating the downstream CYP450 and UGT genes associated with polyphyllin biosynthesis. Genomes enrichment analyses of differentially expressed genes indicated that inoculation with LgD2 and TPB played a positive role in promoting the defense against pathogenic bacteria, enhancing the biosynthesis of carbohydrates, attenuating the process of nitrogen metabolism, and maintaining the equilibrium of the redox reaction homeostasis, potentially indirectly enhancing the polyphyllin yield of P. polyphylla. By combining differentially expressed genes screening, WGCNA, and phylogenetic tree analyses, 17 CYP450 and 2 UGT candidate genes involved in the biosynthesis of polyphyllin I, polyphyllin II, polyphyllin VII, polyphyllin D, and polyphyllin H were identified. These results suggest that endophytes probably effectively promote the accumulation of polyphyllin by regulating key downstream genes in biosynthetic pathways.DiscussionThis study provides a new approach for investigating the regulatory mechanisms of endophytes that promote the production and accumulation of polyphyllin in P. polyphylla, providing a basis for further elucidating the mechanisms of plant-endophyte interactions.

Project description:BackgroundParis polyphylla var. yunnanensis (PPY) is commonly used in traditional Chinese medicine formulas and folk families. Nearly more than 100 chemical substances with medicinal values have been reported in PPY, among which steroidal saponins are the main active components. Due to its long growth cycle, the resource of PPY has become too scarce, and the current production capacity of PPY is still far from meeting the market demand. Numerous studies have shown that endophytic bacteria not only promote the production of secondary metabolites in the host plant, but some of them are also able to produce the same secondary metabolites as the host. However, little is known about the endophytic bacteria associated with PPY in different geographic conditions and tissues. In order to compare the endophytic bacterial communities associated with PPY in different geographic conditions and plant tissues, the endophytic bacteria from roots, stems, and leaves of PPY collected from five locations were isolated, and the diversity, richness, and homogeneity of bacterial communities were analyzed, and the dominant genera correlation with polyphyllin content was further investigated.ResultsA total of 268 endophytic bacterial strains were isolated and identified from PPY. The experimental results showed that the isolates belonged to 5 phyla, 7 classes, 14 orders and 39 genera of bacteria, of which the dominant order was Bacillariophyta and the dominant genera were Bacillus, Pseudomonas and Agrobacterium. In general, the differences in the distribution pattern and diversity of endophytic bacteria in PPY were characterized by the highest diversity and richness index of endophytic bacterial communities in Er yuan Qisheng (QS) and the highest evenness index in Dali Fengyi (FY). The diversity, richness and evenness of bacterial communities in terms of tissue state showed a hierarchical pattern of root > stem > leaf. The three optimal genera were positively correlated with polyphyllin content.ConclusionThe distribution pattern and diversity of endophytic bacteria in PPY were influenced by tissue type and habitat. In addition, three endophytic bacteria (Pseudomonas, Bacllius and Agrobacterium) were positively correlated with the content of polyphylin.

Project description:BackgroundPolyphyllins are significant medicinal compounds found in Paris species, with different polyphyllins fulfilling distinct medicinal roles. Although some genes involved in polyphyllin synthesis have been identified, further exploration of the genes in the polyphyllin synthesis pathway is necessary due to the extensive genome of Paris species. The content and composition of polyphyllins vary among different Paris species, and the variations in specific polyphyllin levels across these plants make them promising candidates for identifying metabolites and genes associated with the biosynthesis of specific polyphyllins.ResultsIn this study, we investigate the global metabolic and transcriptomic profiles of three types of Paris polyphylla var. yunnanensis (Franch.) Hand.-Mazz, one Paris fargesii Franch, and one Paris forrestii (Takht.) H. Li. The rhizome of P. polyphylla is rich in polyphyllin I and II, while P. forrestii is abundant in polyphyllin III, and P. fargesii contains high levels of polyphyllin VI, VII and H. The three Paris species exhibit distinct metabolomic and transcriptomic profiles. Through an integrated analysis of metabolic and transcriptomic data, along with a phylogenetic analysis of genes related to polyphyllin synthesis in Paris, we annotated a total of six 2,3-oxidosqualene cyclases (OSCs), 120 cytochrome P450s (CYPs), and 138 UDP glycosyltransferases (UGTs). Phylogenetic tree analysis of the obtained data assisted in refining the candidate gene pool for OSC, CYP, and UGT. Subsequently, we identified 6, 12, and 26 candidate genes for OSC, CYP, and UGT, respectively. Finally, by combining the analyses of metabolic and genetic differences, we identified a total of 17 candidate genes, including 2 CAS, 4 CYP, and 11 UGT.ConclusionsP. fargesii and P. forrestii are candidate medicinal plants for the development and application of specific polyphyllins. Transcripts from the UGT91 subfamily in Paris may play dual roles, contributing to both the synthesis of polyphyllin II and the catabolism of polyphyllin V and VI. The homologous genes of PpUGT73CE1 may regulate the synthesis of polyphyllin VI in P. fargesii. This study provides new insights into the investigation of biosynthetic pathways in medicinal plants that lack gene clusters.

Dataset Information

RNA-Seq analysis reveals the important co-expressed genes associated with polyphyllin biosynthesis during the developmental stages of Paris polyphylla.

Background

Results

Conclusions

Publications

RNA-Seq analysis reveals the important co-expressed genes associated with polyphyllin biosynthesis during the developmental stages of Paris polyphylla.

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