OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature

Tang, Yongyan; Gao, Chun-Chun; Gao, Ying; Yang, Ying; Shi, Boyang; Yu, Jiali; Lyu, Cong; Sun, Bao‐Fa; Wang, Hailin; Xu, Yunyuan; Yang, Yun‐Gui; Chong, Kang

doi:10.1016/j.devcel.2020.03.009

Cited by 108 publications

(111 citation statements)

References 95 publications

(128 reference statements)

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“…Owing to the high‐throughput sequencing technologies, m 5 C methylome has been profiled in multiple species and different distribution patterns have been identified. In plants (rice, Arabidopsis thaliana ) and mammalian cell/tissues (mouse, human), m 5 Cs are mainly located in coding sequence (CDS) region, and enriched around the translation initiation codon (Amort et al, 2017; Tang et al, 2020; Yang et al, 2017; Yang, Perrera, et al, 2019). A different distribution pattern was also reported in zebrafish embryo where the m 5 C sites were observed to be widely distributed along whole CDS region without any specific enrichment regions (Yang, Wang, et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Recently, a large number of studies have revealed the multiple molecular functions of m 5 C in RNA processing, such as mRNA export (Yang et al, 2017), RNA stability (Chen, Li, et al, 2019; Gigova, Duggimpudi, Pollex, Schaefer, & Koš, 2014; Väre, Eruysal, Narendran, Sarachan, & Agris, 2017; Yang, Wang, et al, 2019), translation (Janin et al, 2019; Tuorto et al, 2012), and long‐distance RNA transport of plant (Yang, Perrera, et al, 2019). Besides, RNA m 5 C modification also plays a vital role in mitochondrial activity (Haag et al, 2016), stress response (Janin et al, 2019; Tang et al, 2020), gametogenesis and embryogenesis (Cui et al, 2017; Hussain, Tuorto, et al, 2013; Yang, Wang, et al, 2019), nerve and brain development (Flores et al, 2017), and multifarious tumorigenesis and migration (Chen, Li, et al, 2019; Liang, Lin, Du, Qiu, & Zhang, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Dynamic transcriptomic m⁵C and its regulatory role in RNA processing

et al. 2021

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RNA 5‐methylcytosine (m5C) is a prevalent RNA modification in multiple RNA species, including messenger RNAs (mRNAs), transfer RNAs (tRNAs), ribosomal RNAs (rRNAs), and noncoding RNAs (ncRNAs), and broadly distributed from archaea, prokaryotes to eukaryotes. The multiple detecting techniques of m5C have been developed, such as m5C‐RIP‐seq, miCLIP‐seq, AZA‐IP‐seq, RNA‐BisSeq, TAWO‐seq, and Nanopore sequencing. These high‐throughput techniques, combined with corresponding analysis pipeline, provide a precise m5C landscape contributing to the deciphering of its biological functions. The m5C modification is distributed along with mRNA and enriched around 5′UTR and 3′UTR, and conserved in tRNAs and rRNAs. It is dynamically regulated by its related enzymes, including methyltransferases (NSUN, DNMT, and TRDMT family members), demethylases (TET families and ALKBH1), and binding proteins (ALYREF and YBX1). So far, accumulative studies have revealed that m5C participates in a variety of RNA metabolism, including mRNA export, RNA stability, and translation. Depletion of m5C modification in the organism could cause dysfunction of mitochondria, drawback of stress response, frustration of gametogenesis and embryogenesis, abnormality of neuro and brain development, and has been implicated in cell migration and tumorigenesis. In this review, we provide a comprehensive summary of dynamic regulatory elements of RNA m5C, including methyltransferases (writers), demethylases (erasers), and binding proteins (readers). We also summarized the related detecting technologies and biological functions of the RNA 5‐methylcytosine, and provided future perspectives in m5C research. This article is categorized under: RNA Processing > RNA Editing and Modification

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dynamic transcriptomic m⁵C and its regulatory role in RNA processing

et al. 2021

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“…Evidently, the alkbh6 mutants showed a lower survival rate than wild-type plants under drought or heat stress, but a higher survival rate than the wild-type under salt stress ( Figure 2 , Figure 3 and Figure 4 ), indicating that ALKBH6 mediates different roles in the Arabidopsis response to various abiotic stresses. The importance of RNA methylation in stress responses in plants has been demonstrated in only a few cases; OsNUSN2, an mRNA m 5 C methyltransferase in rice, was shown to regulate mRNA translation and maintain chloroplast function, which enhances rice adaptation to heat stress [ 44 ], and m 6 A methylation was associated with the stabilization of the transcripts encoding salt response proteins in response to salt stress [ 45 ]. Although we do not know the mechanistic role of ALKBH6 in stress responses, our current results together with these previous findings point to the crucial role of RNA methylation/demethylation in the response of plants to abiotic stresses.…”

Section: Discussionmentioning

confidence: 99%

Functional Characterization of a Putative RNA Demethylase ALKBH6 in Arabidopsis Growth and Abiotic Stress Responses

Hương

Ngoc

Kang

2020

IJMS

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RNA methylation and demethylation, which is mediated by RNA methyltransferases (referred to as “writers”) and demethylases (referred to as “erasers”), respectively, are emerging as a key regulatory process in plant development and stress responses. Although several studies have shown that AlkB homolog (ALKBH) proteins are potential RNA demethylases, the function of most ALKBHs is yet to be determined. The Arabidopsis thaliana genome contains thirteen genes encoding ALKBH proteins, the functions of which are largely unknown. In this study, we characterized the function of a potential eraser protein, ALKBH6 (At4g20350), during seed germination and seedling growth in Arabidopsis under abiotic stresses. The seeds of T-DNA insertion alkbh6 knockdown mutants germinated faster than the wild-type seeds under cold, salt, or abscisic acid (ABA) treatment conditions but not under dehydration stress conditions. Although no differences in seedling and root growth were observed between the alkbh6 mutant and wild-type under normal conditions, the alkbh6 mutant showed a much lower survival rate than the wild-type under salt, drought, or heat stress. Cotyledon greening of the alkbh6 mutants was much higher than that of the wild-type upon ABA application. Moreover, the transcript levels of ABA signaling-related genes, including ABI3 and ABI4, were down-regulated in the alkbh6 mutant compared to wild-type plants. Importantly, the ALKBH6 protein had an ability to bind to both m6A-labeled and m5C-labeled RNAs. Collectively, these results indicate that the potential eraser ALKBH6 plays important roles in seed germination, seedling growth, and survival of Arabidopsis under abiotic stresses.

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“…While recently it has been reported that viral ncRNA level increased followed by the loss of m 5 C modification, which was mediated by the ablation of NSUN2 [53] . Latest studies in this year have related m 5 C modification with the regulation of the thermal adaptability in animal and plant cells by regulating the functions of tRNA and mRNA [54] , [55] . A well-described hydroxymethylcytosine (hm5C) modification in DNAs was also observed in RNAs, which is oxidized form of m 5 C exhibiting important physiological roles in drosophila [56] .…”

Section: Introductionmentioning

confidence: 99%

Bioinformatics approaches for deciphering the epitranscriptome: Recent progress and emerging topics

Song

Zhang

et al. 2020

Computational and Structural Biotechnology Journal

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Post-transcriptional RNA modification occurs on all types of RNA and plays a vital role in regulating every aspect of RNA function. Thanks to the development of high-throughput sequencing technologies, transcriptome-wide profiling of RNA modifications has been made possible. With the accumulation of a large number of high-throughput datasets, bioinformatics approaches have become increasing critical for unraveling the epitranscriptome. We review here the recent progress in bioinformatics approaches for deciphering the epitranscriptomes, including epitranscriptome data analysis techniques, RNA modification databases, disease-association inference, general functional annotation, and studies on RNA modification site prediction. We also discuss the limitations of existing approaches and offer some future perspectives.

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OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature

Abstract: Highlights d OsNSUN2 is the major mRNA m 5 C methyltransferase in rice d m 5 C regulates mRNA translation d m 5 C modulates chloroplast homeostasis d m 5 C enhances rice adaptation to high temperature

Cited by 108 publications

References 95 publications

Dynamic transcriptomic m⁵C and its regulatory role in RNA processing

Dynamic transcriptomic m⁵C and its regulatory role in RNA processing

Functional Characterization of a Putative RNA Demethylase ALKBH6 in Arabidopsis Growth and Abiotic Stress Responses

Bioinformatics approaches for deciphering the epitranscriptome: Recent progress and emerging topics

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OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature

Abstract: Highlights d OsNSUN2 is the major mRNA m 5 C methyltransferase in rice d m 5 C regulates mRNA translation d m 5 C modulates chloroplast homeostasis d m 5 C enhances rice adaptation to high temperature

Cited by 108 publications

References 95 publications

Dynamic transcriptomic m5C and its regulatory role in RNA processing

Dynamic transcriptomic m5C and its regulatory role in RNA processing

Functional Characterization of a Putative RNA Demethylase ALKBH6 in Arabidopsis Growth and Abiotic Stress Responses

Bioinformatics approaches for deciphering the epitranscriptome: Recent progress and emerging topics

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Dynamic transcriptomic m⁵C and its regulatory role in RNA processing

Dynamic transcriptomic m⁵C and its regulatory role in RNA processing