Abstract
The Amaryllidaceae alkaloid galanthamine (Gal) in Lycoris longituba is a secondary metabolite that has been used to treat Alzheimer’s disease. Plant secondary metabolism is affected by methyl jasmonate (MeJA) exposure, although the regulatory mechanisms of MeJA on L. longituba seedlings remains largely unknown. In the present study, 75, 150, and 300 μM MeJA were used as treatments on L. longituba seedlings for 7, 14, 21, and 28 days, while 0 μM MeJA was used as the control (MJ-0). The effect of exogenous MeJA on Gal synthesis in L. longituba was then investigated using transcriptomic sequencing and metabolite profiling via GC-MS and LC-MS analysis. Galanthamine (Gal), lycorine (Lyc), and lycoramine (Lycm) abundances were 2. 71-, 2. 01-, and 2.85-fold higher in 75 μM MeJA (MJ-75) treatment plants compared to MJ-0 treatment plants after 7 days of cultivation. Transcriptomic analysis further showed that MJ-75 treatment significantly induced the expression of norbelladine synthase (NBS) and norbelladine 4′-O-methyltransferase (OMT), which are involved in the Gal biosynthesis pathway. In addition, increased expression was observed in MJ-75 treatment plants for genes in the JA synthesis and JA signaling pathways including those of allene oxide cyclase (AOC), 12-oxo-phytodienoic acid reductase (OPR), jasmonic acid amino acid synthase (JAR), and transcription factor MYC. The L. longituba tyrosine decarboxylase (LlTYDC) enzyme was identified and proposed to be involved in the Gal biosynthetic pathway. Metabolomics results demonstrated that the accumulation of Amaryllidaceae alkaloids, and especially alkaloids in the Gal biosynthesis pathway, could be induced by MJ-75 treatment. Interestingly, metabolites in the JA synthesis pathway were also affected by MeJA treatment. Overall, this multi-omics study suggests that both the JA synthesis/JA signaling and Gal biosynthesis pathways were affected by exogenous MeJA treatment. This comprehensive study of gene expression and metabolite contents can help us better understand the molecular mechanisms underlying MeJA-mediated Gal biosynthesis in L. longituba.
Highlights
Plants of the Lycoris genus, and especially Lycoris longituba, are ornamental flowers and traditional Chinese medicinal herbs used to treat sore throats, carbuncles, and edema (Howes and Houghton, 2003; Wu et al, 2008)
The above data indicate that seedling growth and alkaloid accumulations are all improved by MJ-75 treatment after 7 days
Transcriptome sequencing, GC-Murashige and Skoog (MS), and LC-MS analyses were used to investigate the effects of exogenous methyl jasmonate (MeJA) application on galanthamine (Gal) synthesis in L. longituba
Summary
Plants of the Lycoris genus, and especially Lycoris longituba, are ornamental flowers and traditional Chinese medicinal herbs used to treat sore throats, carbuncles, and edema (Howes and Houghton, 2003; Wu et al, 2008). Six hundred Amaryllidaceae alkaloids, including galanthamine (Gal), lycoramine (Lycm), and lycorine (Lyc), have been identified from the Amaryllidaceae plant family (Jin and Yao, 2019; Desgagné-Penix, 2020). Their pharmacological uses have been reported to include acetylcholinesterase inhibition, cytotoxicity, antibacterial effects, antiviral effects, anti-inflammatory activities, and anticancer effects, among others (Liu et al, 2004; Kornienko and Evidente, 2008; Wang et al, 2010; Kilgore et al, 2016; Hotchandani and Desgagne-Penix, 2017; Pellegrino et al, 2018). Comprehensive understandings of the pathway and Gal accumulation pattern in Lycoris are still lacking
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