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Deciphering the epitranscriptome： A green perspective

Journal of Integrative Plant Biology 2016年第10期58卷 822-835页

作者： Alice Burgess School of Biological Sciences The University of Adelaide South Australia 5005 Australia School of Agriculture Food and Wine The WaiteResearch Institute The University of Adelaide South Australia 5005 Australia The University of Adelaide and Shanghai Jiao Tong University Joint International Centre for Agriculture and Health Joint International Research Laboratory of Metabolic & Developmental Sciences AdelaideAustralia

The advent of high-throughput sequencing technol- ogies coupled with new detection methods of RNA modifica- tions has enabled investigation of a new layer of gene regulation - the epitranscriptome. With over loo known RNA modifications, understanding the repertoire of RNA modifications is a huge undertaking. This review summarizes what is known about RNA modifications with an emphasis on discoveries in plants. RNA ribose modifications, base methyl- ations and pseudouridylation are required for normal develop- ment in Arabidopsis, as mutations in the enzymes modifying them have diverse effects on plant development and stress responses. These modifications can regulate RNA structure, turnover and translation. Transfer RNA and ribosomal RNA modifications have been mapped extensively and their functions investigated in many organisms, including plants. Recent work exploring the locations, functions and targeting of N6-methyladenosine （m^6A）, 5-methylcytosine （m^5C）, pseudour- idine （up）, and additional modifications in mRNAs and ncRNAs are highlighted, as well as those previously known on tRNAs and rRNAs. Many questions remain as to the exact mechanisms of targeting and functions of specific modified sites and whether these modifications have distinct functions in the different classes of RNAs.

关键词： RNA modifications epitranscriptome RNA 5-methylcytosine （m^5C） N^6-methyladenosine （m^6A） Pseudouridine （φ） Arabidopsis

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RNA Methylome Reveals the m^(6)A-mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-withering

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Genomics, Proteomics & Bioinformatics 2023年第4期21卷 769-787页

作者： Chen Zhu Shuting Zhang Chengzhe Zhou Caiyun Tian Biying Shi Kai Xu Linjie Huang Yun Sun Yuling Lin Zhongxiong Lai Yuqiong Guo College of Horticulture Fujian Agriculture and Forestry UniversityFuzhou 350002China Institute of Horticultural Biotechnology Fujian Agriculture and Forestry UniversityFuzhou 350002China Tea Industry Research Institute Fujian Agriculture and Forestry UniversityFuzhou 350002China

The epitranscriptomic mark N6-methyladenosine(m^(6)A),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 m^(6)A-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 m^(6)Amediated regulatory mechanism and its effects on flavonoid and terpenoid metabolism in tea(Camellia sinensis)leaves under solar-withering conditions.Dynamic changes in global m^(6)A level in tea leaves were mainly controlled by two m^(6)A erasers(CsALKBH4A and CsALKBH4B)during solar-withering treatments.Differentially methylated peak-associated genes following solarwithering 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 m^(6)A-mediated regulatory mechanism and the formation of tea flavor under solar-withering conditions.

关键词： Camellia sinensis RNA methylation epitranscriptome Secondary metabolite Withering

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Single-base resolution mapping of 2′-O-methylation sites by an exoribonuclease-enriched chemical method

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Science China(Life Sciences) 2023年第4期66卷 800-818页

作者： Ping Zhang Junhong Huang Wujian Zheng Lifan Chen Shurong Liu Anrui Liu Jiayi Ye Jie Zhou Zhirong Chen Qiaojuan Huang Shun Liu Keren Zhou Lianghu Qu Bin Li Jianhua Yang MOE Key Laboratory of Gene Function and Regulation State Key Laboratory of BiocontrolSchool of Life SciencesThe Fifth Affiliated HospitalSun Yat-sen UniversityGuangzhou 510275China Department of Chemistry The University of ChicagoChicagoIL 60637USA Department of Systems Biology Beckman Research Institute of City of HopeMonroviaCA 91016USA

2′-O-methylation(Nm)is one of the most abundant RNA epigenetic modifications and plays a vital role in the post-transcriptional regulation of gene expression.Current Nm mapping approaches are normally limited to highly abundant RNAs and have significant technical hurdles in m RNAs or relatively rare non-coding RNAs(nc RNAs).Here,we developed a new method for enriching Nm sites by using RNA exoribonuclease and periodate oxidation reactivity to eliminate 2′-hydroxylated(2′-OH)nucleosides,coupled with sequencing(Nm-REP-seq).We revealed several novel classes of Nm-containing nc RNAs as well as m RNAs in humans,mice,and drosophila.We found that some novel Nm sites are present at fixed positions in different t RNAs and are potential substrates of fibrillarin(FBL)methyltransferase mediated by sno RNAs.Importantly,we discovered,for the first time,that Nm located at the 3′-end of various types of nc RNAs and fragments derived from them.Our approach precisely redefines the genome-wide distribution of Nm and provides new technologies for functional studies of Nm-mediated gene regulation.

关键词： 2′-O-methylation MgR exoribonuclease periodate oxidation epitranscriptome transcriptome

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Transcriptome-wide profiling of RNA N^(4)-cytidine acetylation in Arabidopsis thaliana and Oryza sativa

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Molecular Plant 2023年第6期16卷 1082-1098页

作者： Bin Li Donghao Li Linjun Cai Qiting Zhou Cong Liu Jianzhong Lin Yixing Li Xiaoying Zhao Li Li Xuanming Liu Chongsheng He College of Biology Hunan Key Laboratory of Plant Functional Genomics and Developmental RegulationHunan Engineering and Technology Research Center of Hybrid RapeseedHunan UniversityChangsha410082 Hunan 410082China State Key Laboratory of Hybrid Rice Hunan Hybrid Rice Research CenterHunan Academy of Agricultural SciencesChangshaChina

Acetylation of N^(4)-cytidine(ac^(4)C)has recently been discovered as a novel modification of mRNA.RNA ac^(4)C modification has been shown to be a key regulator of RNA stability,RNA translation,and the thermal stress response.However,its existence in eukaryotic mRNAs is still controversial.In plants,the existence,distribution pattern,and potential function of RNA ac^(4)C modification are largely unknown.Here we report the presence of ac^(4)C in the mRNAs of both Arabidopsis thaliana and rice(Oryza sativa).By comparing two ac^(4)C sequencing methods,we found that RNA immunoprecipitation and sequencing(acRIP-seq),but not ac^(4)C sequencing,was suitable for plant RNA ac^(4)C sequencing.We present transcriptome-wide atlases of RNA ac^(4)C modification in A.thaliana and rice mRNAs obtained by acRIP-seq.Analysis of the distribution of RNA ac^(4)C modifications showed that ac^(4)C is enriched near translation start sites in rice mRNAs and near translation start sites and translation end sites in Arabidopsis mRNAs.The RNA ac^(4)C modification level is positively correlated with RNA half-life and the number of splicing variants.Similar to that in mammals,the translation efficiency of ac^(4)C target genes is significantly higher than that of other genes.Our in vitro translation results confirmed that RNA ac^(4)C modification enhances translation efficiency.We also found that RNA ac^(4)C modification is negatively correlated with RNA structure.These results suggest that ac^(4)C is a conserved mRNA modification in plants that contributes to RNA stability,splicing,translation,and secondary structure formation.

关键词： N^(4)-acetylcytidine epitranscriptome Arabidopsis thaliana Oryza sativa

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Reversible RNA Modification N^1-methyladenosine(m^1A) in mRNA and tRNA

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Genomics, Proteomics & Bioinformatics 2018年第3期16卷 155-161页

作者： Chi Zhang Guifang Jia Synthetic and Functional Biomolecules Center Beijing National Laboratory for Molecular Sciences Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education College of Chemistry and Molecular EngineeringPeking University

More than 100 modifications have been found in RNA. Analogous to epigenetic DNA methylation, epitranscriptomic modifications can be written, read, and erased by a complex network of proteins. Apart from Na-methyladenosine （m6A）, N1-methyladenosine （mXA） has been found as a reversible modification in tRNA and mRNA. mlA occurs at positions 9, 14, and 58 of tRNA, with m1A58 being critical for tRNA stability. Other than the hundreds of m1A sites in mRNA and long non-coding RNA transcripts, transcriptome-wide mapping of m1A also identifies 〉 20 m1A sites in mitochondrial genes, m1A in the coding region of mitochondrial transcripts can inhibit the translation of the corresponding proteins. In this review, we summarize the current understanding of mlA in mRNA and tRNA, covering high-throughput sequencing methods developed for m1A methylome, m1A-related enzymes （writers and erasers）, as well as its functions in mRNA and tRNA.

关键词： epitranscriptome RNA modification N1-methyladenosine （m1A） m1A writer m1A eraser

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YTH Domain： A Family of N^6-methyladenosine (m^6A) Readers

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Genomics, Proteomics & Bioinformatics 2018年第2期16卷 99-107页

作者： Shanhui Liao Hongbin Sun Chao Xu Heifei National Laboratory for Physical Sciences at the Microscale and Technology of China Hefei 230027 China School of Food and Biological Engineering Zhengzhou University of Light Industry Zhengzhou 450002 China CAS Key Laboratory of Structural Biology University of Science and Technology of China Hefei 230027 China

Like protein and DNA, different types of RNA molecules undergo various modifications. Accumulating evidence suggests that these RNA modifications serve as sophisticated codes to mediate RNA behaviors and many important biological functions. N^6-methyladenosine （m^6A） is the most abundant internal RNA modification found in a variety of eukaryotic RNAs, including but not limited to mRNAs, tRNAs, rRNAs, and long non-coding RNAs （lncRNAs）. In mammalian cells, m^6A can be incorporated by a methyltransferase complex and removed by demethy- lases, which ensures that the m^6A modification is reversible and dynamic. Moreover, m^6A is recognized by the YT521-B homology （YTH） domain-containing proteins, which subsequently direct different complexes to regulate RNA signaling pathways, such as RNA metabolism, RNA splicing, RNA folding, and protein translation. Herein, we summarize the recent progresses made in understanding the molecular mechanisms underlying the m^6A recognition by YTH domaincontaining proteins, which would shed new light on m^6A-specific recognition and provide clues to the future identification of reader proteins of many other RNA modifications.

关键词： RNA modification RNA methylation RNA demethylation YT521-B homology epitranscriptome

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Comparative Analysis of Human Genes Frequently and Occasionally Regulated by m^6A Modification

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Genomics, Proteomics & Bioinformatics 2018年第2期16卷 127-135页

作者： Yuan Zhou Qinghua Cui Department of Biomedical Informatics School of Basic Medical Sciences Peking University

The m^6A modification has been implicated as an important epitranscriptomic marker, which plays extensive roles in the regulation of transcript stability, splicing, translation, and localization. Nevertheless, only some genes are repeatedly modified across various conditions and the principle of m^6A regulation remains elusive. In this study, we performed a systems-level analysis of human genes frequently regulated by m^6A modification （m^6Afreq genes） and those occasionally regulated by m^6A modification （m^6Aocca genes）. Compared to the m^6Aocca genes, the m^6Afreq genes exhibit gene importance-related features, such as lower dN/dS ratio, higher protein-protein interaction network degree, and reduced tissue expression specificity. Signaling network analysis indicates that the m^6Afreq genes are associated with downstream components of signaling cascades, high-linked signaling adaptors, and specific network motifs like incoherent feed forward loops. Moreover, functional enrichment analysis indicates significant overlaps between the m^6Afreq genes and genes involved in various layers of gene expression, such as being the microRNA targets and the regulators of RNA processing. Therefore, our findings suggest the potential interplay between m^6A epitranscriptomic regulation and other gene expression regulatory machineries.

关键词： m^6A epitranscriptome Signaling network Gene expression regulation Gene importance

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epitranscriptome in Plant Biological Regulation

Epitranscriptome in Plant Biological Regulation

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第十届全国化学生物学学术会议

作者： Hong-Chao Duan Lianhuan Wei Guifang Jia Synthetic and Functional Biomolecules Center Beijing National Laboratory for Molecular Sciences Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education College of Chemistry and Molecular Engineering Peking University

m6 A is the most prevalent internal modification in eukaryotic mRNA and preferentially occurs at the consensus sequence [G/A/U][G＞A]m6 AC[U＞A＞C] with a non-stoichiometric ratio. Although it was first found in 1970 s, relative to DNA modifications, the research on m6 A lagged behind due to the lack of detection techniques for RNA modifications. Until 2011, the discovery of FTO as an m6 A-demethylase demonstrates m6 A is a reversible and dynamic RNA modification and reignites investigation of m6 A. In 2012, two research group developed m6 A antibody immunoprecipitation-based sequencing method（termed m6 A-seq or MeRIP） and reported the whole-transcriptomic m6 A maps. m6 A is installed by a methyltransferase complex（writer） with key subunits identified as METTL3（Methyltransferase-like 3）, METTL14 and WTAP（Wilms tumour 1-associating protein）. So far only two m6 A demethylases（eraser）, FTO and ALKBH5（ AlkB homolog 5）, have been characterized. m6 A is recognized by reader proteins（such as YTH family proteins） to regulate RNA fate, including mR NA stability, splicing, nuclear export,translation, primary microRNA processing, and RNA-protein interactions. These processes affect circadian rhythms, stem cell pluripotency, cancer stem cell proliferation, RNA virus infection, sex determination in Drosophila, and so on, revealing that m6 A plays critical roles in various biological processes. However the study of m6 A on mR NA has been limited to the m6 A methyltransferase subunit MTA（the plant homolog of human METTL3, encoded by At4 g10760）in Arabidopsis thaliana. We will discuss our discovery and characterization of reversible m6 A methylation mediated by demethylase in A. thaliana, and noticeable regulatory roles of this RNA demethylase in plant development especially floral transition. Our findings reveal potential broad functions of reversible mR NA methylation in plants.

关键词： epitranscriptome RNA modification N6-methyladenosine（m6A） m6A demethylase

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Detection,regulation,and functions of RNA N^(6)-methyladenosine modification in plants

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Plant Communications 2023年第3期4卷 32-46页

作者： Jun Tang Shuyan Chen Guifang Jia Synthetic and Functional Biomolecules Center Beijing National Laboratory for Molecular SciencesKey Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of EducationCollege of Chemistry and Molecular EngineeringPeking UniversityBeijing 100871China Peking-Tsinghua Center for Life Sciences Beijing 100871China

N6-Methyladenosine(m^(6)A)is the most abundant internal chemical modification in eukaryotic mRNA and plays important roles in gene expression regulation,including transcriptional and post-transcriptional regulation.m^(6)A is a reversible modification that is installed,removed,and recognized by methyltransferases(writers),demethylases(erasers),and m^(6)A-binding proteins(readers),respectively.Recently,the breadth of research on m^(6)A in plants has expanded,and the vital roles of m^(6)A in plant development,biotic and abiotic stress responses,and crop trait improvement have been investigated.In this review,we discuss recent developments in research on m^(6)A and highlight the detection methods,distribution,regulatory proteins,and molecular and biological functions of m^(6)A in plants.We also offer some perspectives on future investigations,providing direction for subsequent research on m^(6)A in plants.

关键词： RNA modification m^(6)A plants epitranscriptome

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