Transcriptome analysis reveals regulation mechanism of methyl jasmonate-induced terpenes biosynthesis in Curcuma wenyujin

Wei, Qiuhui; Lan, Kaer; Liu, Yuyang; Chen, Rong; Hu, Tianyuan; Zhao, Shujuan; Yin, Xia; Xie, Tianqi

doi:10.1371/journal.pone.0270309

Cited by 20 publications

(14 citation statements)

References 56 publications

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“…Increasing evidence has shown that JA synthesis-related genes, e.g., DXS , DXR and OPR3 in P. quinquefolius and Solanum tuberosum L. upregulate their expression levels in response to the induction of R. intraradices and R. irregularis ( Schoenherr et al., 2019 ; Ran et al., 2021b and 2023 ). Wei et al. (2022) confirmed that in Curcuma wenyujin Y. Chen & C. Ling, the expression levels of key enzyme-encoding genes ( LOX , AOS , AOC , OPR , MFP and JAR ) involved in JA biosynthesis and JA signal transduction genes ( MYC2 and JAZ ) increased significantly under MeJA.…”

Section: Discussionsupporting

confidence: 65%

Improvement of Panax notoginseng saponin accumulation triggered by methyl jasmonate under arbuscular mycorrhizal fungi

Dai,

Zhang,

et al. 2024

Front. Plant Sci.

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Panax notoginseng is a highly valued perennial medicinal herb plant in Yunnan Province, China, and the taproots are the main medicinal parts that are rich in active substances of P. notoginseng saponins. The main purpose of this study is to uncover the physiological and molecular mechanism of Panax notoginseng saponin accumulation triggered by methyl jasmonate (MeJA) under arbuscular mycorrhizal fungi (AMF) by determining physiological indices, high-throughput sequencing and correlation analysis. Physiological results showed that the biomass and saponin contents of P. notoginseng, the concentrations of jasmonic acids (JAs) and the key enzyme activities involved in notoginsenoside biosynthesis significantly increased under AMF or MeJA, but the interactive treatment of AMF and MeJA weakened the effect of AMF, suggesting that a high concentration of endogenous JA have inhibitory effect. Transcriptome sequencing results indicated that differential expressed genes (DEGs) involved in notoginsenoside and JA biosynthesis were significantly enriched in response to AMF induction, e.g., upregulated genes of diphosphocytidyl-2-C-methyl-d-erythritol kinases (ISPEs), cytochrome P450 monooxygenases (CYP450s)_and glycosyltransferases (GTs), while treatments AMF-MeJA and salicylhydroxamic acid (SHAM) decreased the abundance of these DEGs. Interestingly, a high correlation presented between any two of saponin contents, key enzyme activities and expression levels of DEGs. Taken together, the inoculation of AMF can improve the growth and saponin accumulation of P. notoginseng by strengthening the activities of key enzymes and the expression levels of encoding genes, in which the JA regulatory pathway is a key link. This study provides references for implementing ecological planting of P. notoginseng, improving saponin accumulation and illustrating the biosynthesis mechanism.

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Section: Discussionsupporting

confidence: 65%

Improvement of Panax notoginseng saponin accumulation triggered by methyl jasmonate under arbuscular mycorrhizal fungi

Dai,

Zhang,

et al. 2024

Front. Plant Sci.

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“…MeJA induces both the production of MVA- and MEP pathway-derived metabolites [ 22 , 42 , 43 ]. With this in mind, we hypothesized that MeJA may affect the metabolic flux leading to the biosynthesis of prenyl diphosphates used to modify proteins.…”

Section: Resultsmentioning

confidence: 99%

Methyl-Jasmonate Functions as a Molecular Switch Promoting Cross-Talk between Pathways for the Biosynthesis of Isoprenoid Backbones Used to Modify Proteins in Plants

Chevalier,

Huchelmann,

Debié

et al. 2024

Plants

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In plants, the plastidial mevalonate (MVA)-independent pathway is required for the modification with geranylgeranyl groups of CaaL-motif proteins, which are substrates of protein geranylgeranyltransferase type-I (PGGT-I). As a consequence, fosmidomycin, a specific inhibitor of 1-deoxy-d-xylulose (DX)-5 phosphate reductoisomerase/DXR, the second enzyme in this so-called methylerythritol phosphate (MEP) pathway, also acts as an effective inhibitor of protein prenylation. This can be visualized in plant cells by confocal microscopy by expressing GFP-CaM-CVIL, a prenylation sensor protein. After treatment with fosmidomycin, the plasma membrane localization of this GFP-based sensor is altered, and a nuclear distribution of fluorescence is observed instead. In tobacco cells, a visual screen of conditions allowing membrane localization in the presence of fosmidomycin identified jasmonic acid methyl esther (MeJA) as a chemical capable of gradually overcoming inhibition. Using Arabidopsis protein prenyltransferase loss-of-function mutant lines expressing GFP-CaM-CVIL proteins, we demonstrated that in the presence of MeJA, protein farnesyltransferase (PFT) can modify the GFP-CaM-CVIL sensor, a substrate the enzyme does not recognize under standard conditions. Similar to MeJA, farnesol and MVA also alter the protein substrate specificity of PFT, whereas DX and geranylgeraniol have limited or no effect. Our data suggest that MeJA adjusts the protein substrate specificity of PFT by promoting a metabolic cross-talk directing the origin of the prenyl group used to modify the protein. MVA, or an MVA-derived metabolite, appears to be a key metabolic intermediate for this change in substrate specificity.

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“…In this study, we found that the expression levels of key enzyme genes ( DXS , DXR , MCT , MCS , and HDS ) for skeleton synthesis were up-regulated under the action of MeJA, which is similar to the studies in Chrysanthemum indicum var. aromaticum [ 61 ], Curcuma wenyujin [ 64 ], and Artemisia annua [ 60 ], indicating that the synthesis of monoterpenoid in S. tenuifolia is mediated by the MEP pathway. In addition, we identified two HDR genes in S. tenuifolia , and the researchers showed that HDR was highly expressed in Artemisia annua [ 57 ] and Salvia miltiorrhiza [ 65 ] after MeJA treatment, but we found that the expression levels of StHDR after MeJA treatment were significantly down-regulated compared with the CK group, and the specific molecular mechanism needs to be further explored.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomics Reveals the Molecular Basis for Methyl Jasmonate to Promote the Synthesis of Monoterpenoids in Schizonepeta tenuifolia Briq.

Shi

Cui

Zhang

et al. 2023

CIMB

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Background: Methyl jasmonate has an important effect on the synthesis of plant secondary metabolites. Schizonepeta tenuifolia Briq. has a wide range of pharmacological effects and the secondary metabolites are dominated by monoterpenes (pulegone, menthone). Objective: It is essential to determine the changes in secondary metabolites in S. tenuifolia under methyl jasmonate treatment and to probe the molecular mechanism. This can improve the accumulation of secondary metabolites in the medicinal plant S. tenuifolia and enrich the information gene expression at different MeJA levels, which can help to elucidate the molecular mechanism of monoterpenoid synthesis in S. tenuifolia. Methods: In this study, we determined the changes in the content of monoterpenoids in S. tenuifolia under methyl jasmonate treatment. Meanwhile, we established a transcriptome database of S. tenuifolia under methyl jasmonate level using high-throughput sequencing. Results: A certain concentration of MeJA promoted the accumulation of monoterpenoids in S. tenuifolia. The transcriptome database of S. tenuifolia leaves under 0, 50, 100 and 250 μM MeJA treatment was established. We generated 88,373 unigenes with an N50 length of 2678 bp, of which 50,843 (57.53%) can be annotated in at least one database. Compared with the CK (0 μM) group, 12,557 (50 μM), 15,409 (100 μM) and 13,286 (250 μM) differentially expressed genes were identified. GO and KEGG enrichment analysis revealed that JA signal transduction and monoterpenoid synthesis were the two most significant enrichment pathways. The expression levels of related DEGs involved in JA signaling and monoterpenoid synthesis were significantly up-regulated by MeJA. In addition, our phenotypic and differentially expressed gene association analysis revealed that monoterpenoid biosynthesis in S. tenuifolia was more associated with genes involved in plant trichome branching, phytohormone signaling and transcriptional regulation. Conclusions: This study confirmed that methyl jasmonate significantly promoted monoterpenoid biosynthesis in S. tenuifolia. A large number of genes responding to methyl jasmonate were associated with JA signaling and monoterpenoid biosynthesis.

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Transcriptome analysis reveals regulation mechanism of methyl jasmonate-induced terpenes biosynthesis in Curcuma wenyujin

Cited by 20 publications

References 56 publications

Improvement of Panax notoginseng saponin accumulation triggered by methyl jasmonate under arbuscular mycorrhizal fungi

Improvement of Panax notoginseng saponin accumulation triggered by methyl jasmonate under arbuscular mycorrhizal fungi

Methyl-Jasmonate Functions as a Molecular Switch Promoting Cross-Talk between Pathways for the Biosynthesis of Isoprenoid Backbones Used to Modify Proteins in Plants

Transcriptomics Reveals the Molecular Basis for Methyl Jasmonate to Promote the Synthesis of Monoterpenoids in Schizonepeta tenuifolia Briq.

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