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Early stem growth mutation alters metabolic flux changes enhance sesquiterpenoids biosynthesis in Atractylodes lancea (Thunb.) DC.

ABSTRACT: Atractylodes lancea (Thunb.) DC. is a well-known medicinal herb in China, containing abundant active components, including a variety of sesquiterpenoids. Owing to a shortage of wild resources, artificial cultivation has become the main breeding mode, leading to the germplasm degradation. In preliminary research, our research group found that a mutant tissue culture seedling of A. lancea is an excellent germplasm resource, characterized by early stem growth and higher sesquiterpenoid content than that of the wild type. In this study, the physiological and biochemical mechanisms underlying efficient sesquiterpenoids synthesis by this mutant A. lancea were systematically evaluated. The results showed that the photosynthetic efficiency, central carbon metabolism efficiency, and energy metabolism efficiency were significantly improved in mutant A. lancea compared with the wild type, and the content of endogenous hormones, such as gibberellin and jasmonic acid, changed significantly. In addition, levels of key metabolites and the expression level of key genes in the mevalonate and 2-C-methyl-d-erythritol-4-phosphate pathways were significantly higher in mutant type than in wild type, resulting in elevated sesquiterpenoid synthesis in the mutant. These physiological and biochemical properties explain the rapid growth and high sesquiterpenoid content of mutant A. lancea.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11240-022-02240-5. Key message Efficient sesquiterpenoids synthesis in early stem growth mutation of Atractylodes lancea could be explained by the biological activities enhancement and up-regulation of sesquiterpene synthesis pathway via gibberellin and jasmonic acid.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11240-022-02240-5.

SUBMITTER: Wang D

PROVIDER: S-EPMC8806136 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Atractylodes lancea (Thunb.) DC. (AL) has been indicated in traditional prescriptions for the treatment of depression. However, the mechanism of action of AL in the treatment of depression is still unclear. This study aimed to investigate the antidepressant potential of AL using network pharmacology, molecular docking, and animal experiments. The active components of AL were retrieved from the traditional Chinese medicine systems pharmacology database and analysis platform (TCMSP), and the depression-related targets were screened through the DisGeNET database. Overlapping targets of AL and depression were selected and analyzed. Ten active compounds of AL showed anti-depressant potential, including stigmasterol, 3β-acetoxyatractylone, wogonin, β-sitosterol, selina-4(14),7(11)-dien-8-one, atractylenolide I, atractylenolide II, atractylenolide III, patchoulene, and cyperene. These compounds target 28 potential antidepressant genes/proteins. Gene Ontology (GO) enrichment analysis revealed that the potential targets might directly influence neural cells and regulate neuroinflammation and neurotransmitter-related processes. The potential Kyoto Encyclopedia Genes and Genomes (KEGG) pathways for the antidepressant effects of AL include neuroactive ligand-receptor interactions, calcium signaling pathways, dopaminergic synapse, interleukin (IL)-17 signaling pathways, and the pathways of neurodegeneration. IL-6, nitric oxide synthase 3 (NOS), solute carrier family 6 member 4 (SLC6A4), estrogen receptor (ESR1), and tumor necrosis factor (TNF) were the most important proteins in the protein-protein interaction network and these proteins showed high binding affinities with the corresponding AL compounds. AL showed an antidepressant effect in mice by decreasing immobility time in the tail suspension test and increasing the total contact number in the social interaction test. This study demonstrated the antidepressant potential of AL, which provides evidence for pursuing further studies to develop a novel antidepressant.

Project description:Ethylene, the first known gaseous phytohormone, is involved in plant growth, development as well as responses to environmental signals. However, limited information is available on the role of ethylene in endophytic fungi induced secondary metabolites biosynthesis. Atractylodes lancea is a traditional Chinese herb, and its quality depends on the main active compounds sesquiterpenoids. This work showed that the endophytic fungus Gilmaniella sp. AL12 induced ethylene production in Atractylodes lancea. Pre-treatment of plantlets with ethylene inhibiter aminooxyacetic acid (AOA) suppressed endophytic fungi induced accumulation of ethylene and sesquiterpenoids. Plantlets were further treated with AOA, salicylic acid (SA) biosynthesis inhibitor paclobutrazol (PAC), jasmonic acid inhibitor ibuprofen (IBU), hydrogen peroxide (H2O2) scavenger catalase (CAT), nitric oxide (NO)-specific scavenger 2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (cPTIO). With endophytic fungi inoculation, IBU or PAC did not inhibit ethylene production, and JA and SA generation were suppressed by AOA, showing that ethylene may act as an upstream signal of JA and SA pathway. With endophytic fungi inoculation, CAT or cPTIO suppressed ethylene production, and H2O2 or NO generation was not affected by 1-aminocyclopropane-1-carboxylic acid (ACC), showing that ethylene may act as a downstream signal of H2O2 and NO pathway. Then, plantlets were treated with ethylene donor ACC, JA, SA, H2O2, NO donor sodium nitroprusside (SNP). Exogenous ACC could trigger JA and SA generation, whereas exogenous JA or SA did not affect ethylene production, and the induced sesquiterpenoids accumulation triggered by ACC was partly suppressed by IBU and PAC, showing that ethylene acted as an upstream signal of JA and SA pathway. Exogenous ACC did not affect H2O2 or NO generation, whereas exogenous H2O2 and SNP induced ethylene production, and the induced sesquiterpenoids accumulation triggered by SNP or H2O2 was partly suppressed by ACC, showing that ethylene acted as a downstream signal of NO and H2O2 pathway. Taken together, this study demonstrated that ethylene is an upstream signal of JA and SA, and a downstream signal of NO and H2O2 signaling pathways, and acts as an important signal mediating sesquiterpenoids biosynthesis of Atractylodes lancea induced by the endophytic fungus.

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Early stem growth mutation alters metabolic flux changes enhance sesquiterpenoids biosynthesis in Atractylodes lancea (Thunb.) DC.

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