Dataset Information

RNA Methylome Reveals the m⁶A-mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-withering.

ABSTRACT: The epitranscriptomic mark N⁶-methyladenosine (m⁶A), which is the predominant internal modification in RNA, is important for plant responses to diverse stresses. Multiple environmental stresses caused by the tea-withering process can greatly influence the accumulation of specialized metabolites and the formation of tea flavor. However, the effects of the m⁶A-mediated regulatory mechanism on flavor-related metabolic pathways in tea leaves remain relatively uncharacterized. We performed an integrated RNA methylome and transcriptome analysis to explore the m⁶A-mediated regulatory mechanism and its effects on flavonoid and terpenoid metabolism in tea (Camellia sinensis) leaves under solar-withering conditions. Dynamic changes in global m⁶A level in tea leaves were mainly controlled by two m⁶A erasers (CsALKBH4A and CsALKBH4B) during solar-withering treatments. Differentially methylated peak-associated genes following solar-withering treatments with different shading rates were assigned to terpenoid biosynthesis and spliceosome pathways. Further analyses indicated that CsALKBH4-driven RNA demethylation can directly affect the accumulation of volatile terpenoids by mediating the stability and abundance of terpenoid biosynthesis-related transcripts and also indirectly influence the flavonoid, catechin, and theaflavin contents by triggering alternative splicing-mediated regulation. Our findings revealed a novel layer of epitranscriptomic gene regulation in tea flavor-related metabolic pathways and established a link between the m⁶A-mediated regulatory mechanism and the formation of tea flavor under solar-withering conditions.

SUBMITTER: Zhu C

PROVIDER: S-EPMC10787128 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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RNA Methylome Reveals the m6A-mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-withering.

Zhu Chen C Zhang Shuting S Zhou Chengzhe C Tian Caiyun C Shi Biying B Xu Kai K Huang Linjie L Sun Yun Y Lin Yuling Y Lai Zhongxiong Z Guo Yuqiong Y

Genomics, proteomics & bioinformatics 20230214 4

The epitranscriptomic mark N6-methyladenosine (m6A), which is the predominant internal modification in RNA, is important for plant responses to diverse stresses. Multiple environmental stresses caused by the tea-withering process can greatly influence the accumulation of specialized metabolites and the formation of tea flavor. However, the effects of the m6A-mediated regulatory mechanism on flavor-related metabolic pathways in tea leaves remain relatively unchara ...[more]

PMID: 36791953

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Project description:Oolong tea is a popular and semi-fermented beverage. During the processing of tea leaves, withering is the first indispensable process for improving flavor. However, the roles of long non-coding RNAs (lncRNAs) and the characteristic secondary metabolites during the withering of oolong tea leaves remain unknown. In this study, phytochemical analyses indicated that total polyphenols, flavonoids, catechins, epigallocatechin (EGC), catechin gallate (CG), gallocatechin gallate (GCG), epicatechin gallate (ECG), and epigallocatechin gallate (EGCG) were all less abundant in the solar-withered leaves (SW) than in the fresh leaves (FL) and indoor-withered leaves (IW). In contrast, terpenoid, jasmonic acid (JA), and methyl jasmonate (MeJA) contents were higher in the SW than in the FL and IW. By analyzing the transcriptome data, we detected 32,036 lncRNAs. On the basis of the Kyoto Encyclopedia of Genes and Genomes analysis, the flavonoid metabolic pathway, the terpenoid metabolic pathway, and the JA/MeJA biosynthesis and signal transduction pathway were enriched pathways. Additionally, 63 differentially expressed lncRNAs (DE-lncRNAs) and 23 target genes were identified related to the three pathways. A comparison of the expression profiles of the DE-lncRNAs and their target genes between the SW and IW revealed four up-regulated genes (FLS, CCR, CAD, and HCT), seven up-regulated lncRNAs, four down-regulated genes (4CL, CHI, F3H, and F3'H), and three down-regulated lncRNAs related to flavonoid metabolism; nine up-regulated genes (DXS, CMK, HDS, HDR, AACT, MVK, PMK, GGPPS, and TPS), three up-regulated lncRNAs, and six down-regulated lncRNAs related to terpenoid metabolism; as well as six up-regulated genes (LOX, AOS, AOC, OPR, ACX, and MFP2), four up-regulated lncRNAs, and three down-regulated lncRNAs related to JA/MeJA biosynthesis and signal transduction. These results suggested that the expression of DE-lncRNAs and their targets involved in the three pathways may be related to the low abundance of the total polyphenols, flavonoids, and catechins (EGC, CG, GCG, ECG, and EGCG) and the high abundance of terpenoids in the SW. Moreover, solar irradiation, high JA and MeJA contents, and the endogenous target mimic (eTM)-related regulatory mechanism in the SW were also crucial for increasing the terpenoid levels. These findings provide new insights into the greater contribution of solar-withering to the high-quality flavor of oolong tea compared with the effects of indoor-withering.

Project description:BackgroundTea (Camellia sinensis) has long been consumed worldwide for its amazing flavor and aroma. Methyl jasmonate (MeJA), which acts as an effective elicitor among the plant kingdom, could mostly improve the quality of tea aroma by promoting flavor volatiles in tea leaves. Although a variety of volatile secondary metabolites that contribute to aroma quality have been identified, our understanding of the biosynthetic pathways of these compounds has remained largely incomplete. Therefore, information aboaut the transcriptome of tea leaves and, specifically, details of any changes in gene expression in response to MeJA, is required for a better understanding of the biological mechanisms of MeJA-mediated volatiles biosynthesis. Moreover, MeJA treatment could exaggerate the responses of secondary metabolites and some gene expression which offer a better chance to figure out the mechanism.ResultsThe results of two-dimensional gas-chromatograph mass-spectrometry showed that the terpenoids content in MeJA-treated tea leaves increased, especially linalool, geraniol, and phenylethyl alcohol. More importantly, we carried out RNA-seq to identify the differentially expressed genes (DEGs) related to volatiles biosynthesis pathways induced by MeJA treatment (0 h, 12 h, 24 h and 48 h) in tea leaves. We identified 19245, 18614, 11890 DEGs respectively in the MeJA_12h, MeJA_24 h and MeJA_48 h samples. The α-Lenolenic acid degradation pathway was firstly responded resulting in activating the JA-pathway inner tea leaves, and the MEP/DOXP pathway significantly exaggerated. Notably, the expression level of jasmonate O-methyltransferase, which is associated with the central JA biosynthesis pathway, was increased by 7.52-fold in MeJA_24 h tea leaves. Moreover, the genes related to the terpenoid backbone biosynthesis pathway showed different expression patterns compared with the untreated leaves. The expression levels of 1-deoxy-D-xylulose-phosphate synthase (DXS), all-trans-nonaprenyl-diphosphate synthase, geranylgeranyl reductase, geranylgeranyl diphosphate synthase (type II), hydroxymethylglutaryl-CoA reductase and 4-hydroxy-3-methylbut-2-enyl diphosphate reductase increased by approximately 2-4-fold.ConclusionsThe results of two-dimension gas-chromatography mass-spectrometry analysis suggested that exogenous application of MeJA could induce the levels of volatile components in tea leaves, especially the geraniol, linalool and its oxides. Moreover, the transcriptome analysis showed increased expression of genes in α-Lenolenic acid degradation pathway which produced massive jasmonic acid and quickly activated holistic JA-pathway inner tea leaves, also the terpenoid backbones biosynthesis pathway was significantly affected after MeJA treatment. In general, MeJA could greatly activate secondary metabolism pathways, especially volatiles. The results will deeply increase our understanding of the volatile metabolites biosynthesis pathways of tea leaves in response to MeJA.

Dataset Information

RNA Methylome Reveals the m⁶A-mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-withering.

Publications

RNA Methylome Reveals the m<sup>6</sup>A-mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-withering.

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