N4-acetylation of cytidine in mRNA plays essential roles in plants

Wenlei Wang; Huijie Liu; Feifei Wang; Xiaoye Liu; Yu Sun; Jie Zhao; Changhua Zhu; Lijun Gan; Jinping Yu; Claus Peter Witte; Mingjia Chen

doi:10.1093/plcell/koad189

N4-acetylation of cytidine in mRNA plays essential roles in plants

Wenlei Wang
, Huijie Liu
, Feifei Wang
, Xiaoye Liu
, Yu Sun
, Jie Zhao
, Changhua Zhu
, Lijun Gan
, Jinping Yu
, Claus Peter Witte
, Mingjia Chen^*

^*Korrespondierende*r Autor*in für diese Arbeit

Institut für Pflanzenernährung

Publikation: Beitrag in Fachzeitschrift › Artikel › Forschung › Peer-Review

Abstract

The biological function of RNA can be modulated by base modifications. Here, we unveiled the occurrence of N4-acetylation of cytidine in plant RNA, including mRNA, by employing LC-MS/MS and acRIP-seq. We identified 325 acetylated transcripts from the leaves of 4-week-old Arabidopsis (Arabidopsis thaliana) plants and determined that 2 partially redundant N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA (ACYR1 and ACYR2), which are homologous to mammalian NAT10, are required for acetylating RNA in vivo. A double-null mutant was embryo lethal, while eliminating 3 of the 4 ACYR alleles led to defects in leaf development. These phenotypes could be traced back to the reduced acetylation and concomitant destabilization of the transcript of TOUGH, which is required for miRNA processing. These findings indicate that N4-acetylation of cytidine is a modulator of RNA function with a critical role in plant development and likely many other processes.

Originalsprache	Englisch
Seiten (von - bis)	3739-3756
Seitenumfang	18
Fachzeitschrift	PLANT CELL
Jahrgang	35
Ausgabenummer	10
Elektronisch veröffentlicht (E-Pub)	27 Juni 2023
DOIs	https://doi.org/10.1093/plcell/koad189
Publikationsstatus	Veröffentlicht - Okt. 2023

ASJC Scopus Sachgebiete

Pflanzenkunde

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10.1093/plcell/koad189Lizenz: Nicht angegeben

Andere Dateien und Links

Verknüpfung zur Publikation in Scopus

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Dieses zitieren

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title = "N4-acetylation of cytidine in mRNA plays essential roles in plants",

abstract = "The biological function of RNA can be modulated by base modifications. Here, we unveiled the occurrence of N4-acetylation of cytidine in plant RNA, including mRNA, by employing LC-MS/MS and acRIP-seq. We identified 325 acetylated transcripts from the leaves of 4-week-old Arabidopsis (Arabidopsis thaliana) plants and determined that 2 partially redundant N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA (ACYR1 and ACYR2), which are homologous to mammalian NAT10, are required for acetylating RNA in vivo. A double-null mutant was embryo lethal, while eliminating 3 of the 4 ACYR alleles led to defects in leaf development. These phenotypes could be traced back to the reduced acetylation and concomitant destabilization of the transcript of TOUGH, which is required for miRNA processing. These findings indicate that N4-acetylation of cytidine is a modulator of RNA function with a critical role in plant development and likely many other processes.",

author = "Wenlei Wang and Huijie Liu and Feifei Wang and Xiaoye Liu and Yu Sun and Jie Zhao and Changhua Zhu and Lijun Gan and Jinping Yu and Witte, \{Claus Peter\} and Mingjia Chen",

note = "Funding Information: The authors thank Jialei Wang for her help with mass spectrometry analyses, Christel Schmiechen for her assistance with seedling phenotype analyses, and Markus Niehaus for his help with statistical analyses. This work was financially supported by the Fundamental Research Funds for the Central Universities [grant number YDZX2023013]; the National Natural Science Foundation of China [grant number 31900907]; the Natural Science Foundation of Jiangsu Province, China [grant number BK20190528]; the International Centre for Genetic Engineering and Biotechnology [grant number CRP/CHN20-04\_EC]; the Deutsche Forschungsgemeinschaft (DFG) [grant numbers CH2292/1-1 to M.C. and C.-P.W, WI3411/8-1, and INST 187/741-1 FUGG to C.-P.W.]; the Special Fund on Technology Innovation of Carbon Dioxide Peaking and Carbon Neutrality of Jiangsu Province [grant number BE2022306 to J.Y.]; and the start-up fund for advanced talents from Nanjing Agricultural University to M.C. ",

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month = oct,

doi = "10.1093/plcell/koad189",

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volume = "35",

pages = "3739--3756",

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publisher = "American Society of Plant Biologists",

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AU - Wang, Wenlei

AU - Liu, Huijie

AU - Wang, Feifei

AU - Liu, Xiaoye

AU - Sun, Yu

AU - Zhao, Jie

AU - Zhu, Changhua

AU - Gan, Lijun

AU - Yu, Jinping

AU - Witte, Claus Peter

AU - Chen, Mingjia

N1 - Funding Information: The authors thank Jialei Wang for her help with mass spectrometry analyses, Christel Schmiechen for her assistance with seedling phenotype analyses, and Markus Niehaus for his help with statistical analyses. This work was financially supported by the Fundamental Research Funds for the Central Universities [grant number YDZX2023013]; the National Natural Science Foundation of China [grant number 31900907]; the Natural Science Foundation of Jiangsu Province, China [grant number BK20190528]; the International Centre for Genetic Engineering and Biotechnology [grant number CRP/CHN20-04_EC]; the Deutsche Forschungsgemeinschaft (DFG) [grant numbers CH2292/1-1 to M.C. and C.-P.W, WI3411/8-1, and INST 187/741-1 FUGG to C.-P.W.]; the Special Fund on Technology Innovation of Carbon Dioxide Peaking and Carbon Neutrality of Jiangsu Province [grant number BE2022306 to J.Y.]; and the start-up fund for advanced talents from Nanjing Agricultural University to M.C.

PY - 2023/10

Y1 - 2023/10

N2 - The biological function of RNA can be modulated by base modifications. Here, we unveiled the occurrence of N4-acetylation of cytidine in plant RNA, including mRNA, by employing LC-MS/MS and acRIP-seq. We identified 325 acetylated transcripts from the leaves of 4-week-old Arabidopsis (Arabidopsis thaliana) plants and determined that 2 partially redundant N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA (ACYR1 and ACYR2), which are homologous to mammalian NAT10, are required for acetylating RNA in vivo. A double-null mutant was embryo lethal, while eliminating 3 of the 4 ACYR alleles led to defects in leaf development. These phenotypes could be traced back to the reduced acetylation and concomitant destabilization of the transcript of TOUGH, which is required for miRNA processing. These findings indicate that N4-acetylation of cytidine is a modulator of RNA function with a critical role in plant development and likely many other processes.

AB - The biological function of RNA can be modulated by base modifications. Here, we unveiled the occurrence of N4-acetylation of cytidine in plant RNA, including mRNA, by employing LC-MS/MS and acRIP-seq. We identified 325 acetylated transcripts from the leaves of 4-week-old Arabidopsis (Arabidopsis thaliana) plants and determined that 2 partially redundant N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA (ACYR1 and ACYR2), which are homologous to mammalian NAT10, are required for acetylating RNA in vivo. A double-null mutant was embryo lethal, while eliminating 3 of the 4 ACYR alleles led to defects in leaf development. These phenotypes could be traced back to the reduced acetylation and concomitant destabilization of the transcript of TOUGH, which is required for miRNA processing. These findings indicate that N4-acetylation of cytidine is a modulator of RNA function with a critical role in plant development and likely many other processes.

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SN - 1040-4651

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EP - 3756

JO - PLANT CELL

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IS - 10

ER -

N4-acetylation of cytidine in mRNA plays essential roles in plants

Abstract

ASJC Scopus Sachgebiete

Zugriff auf Dokument

Andere Dateien und Links

Projekte

Identifizierung und Charakterisierung von cytosolischen Nukleosid-Monophosphat-Phosphatasen der Pflanzen

Hochauflösendes Massenspektrometer (HRMS) gekoppelt an Ionenchromatographie (IC) oder Flüssigkeitschromatographie (LC)

Der Katabolismus nicht-kanonischer Nukleoside aus RNA-Abbau in Pflanzen

Dieses zitieren