Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings

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 larg...

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Main Authors: Qingzhu Li, Junxu Xu, Yuhong Zheng, Yongchun Zhang, Youming Cai
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.713795/full
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spelling doaj-4cd2dfe2a3854218b4469ad0a6b2a7c42021-09-30T05:22:23ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.713795713795Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba SeedlingsQingzhu Li0Qingzhu Li1Junxu Xu2Yuhong Zheng3Yongchun Zhang4Youming Cai5Forestry and Pomology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Co-Elite Agricultural Sci-Tech (Group) Co., Ltd., Shanghai, ChinaForestry and Pomology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing Botanical Garden, Memorial Sun Yat-sen, Nanjing, ChinaForestry and Pomology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaForestry and Pomology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaThe 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.https://www.frontiersin.org/articles/10.3389/fpls.2021.713795/fullLycoris longitubamethyl jasmonate(MeJA)galanthamine biosynthesistranscriptomicsmetabolometyrosine decarboxylase
collection DOAJ
language English
format Article
sources DOAJ
author Qingzhu Li
Qingzhu Li
Junxu Xu
Yuhong Zheng
Yongchun Zhang
Youming Cai
spellingShingle Qingzhu Li
Qingzhu Li
Junxu Xu
Yuhong Zheng
Yongchun Zhang
Youming Cai
Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
Frontiers in Plant Science
Lycoris longituba
methyl jasmonate(MeJA)
galanthamine biosynthesis
transcriptomics
metabolome
tyrosine decarboxylase
author_facet Qingzhu Li
Qingzhu Li
Junxu Xu
Yuhong Zheng
Yongchun Zhang
Youming Cai
author_sort Qingzhu Li
title Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
title_short Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
title_full Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
title_fullStr Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
title_full_unstemmed Transcriptomic and Metabolomic Analyses Reveals That Exogenous Methyl Jasmonate Regulates Galanthamine Biosynthesis in Lycoris longituba Seedlings
title_sort transcriptomic and metabolomic analyses reveals that exogenous methyl jasmonate regulates galanthamine biosynthesis in lycoris longituba seedlings
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-09-01
description 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.
topic Lycoris longituba
methyl jasmonate(MeJA)
galanthamine biosynthesis
transcriptomics
metabolome
tyrosine decarboxylase
url https://www.frontiersin.org/articles/10.3389/fpls.2021.713795/full
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