Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene

Abstract N4-acetylcytidine (ac4C) modification of mRNA has been shown to be present in plant RNAs, but its regulatory function in plant remains largely unexplored. In this study, we investigated the differentially expressed mRNAs, lncRNAs and acetylation modifications of mRNAs in tomato fruits from...

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Main Authors: Lili Ma, Yanyan Zheng, Zhongjing Zhou, Zhiping Deng, Jinjuan Tan, Chunmei Bai, Anzhen Fu, Qing Wang, Jinhua Zuo
Format: Article
Language:English
Published: BMC 2024-02-01
Series:Molecular Horticulture
Subjects:
Online Access:https://doi.org/10.1186/s43897-024-00082-7
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author Lili Ma
Yanyan Zheng
Zhongjing Zhou
Zhiping Deng
Jinjuan Tan
Chunmei Bai
Anzhen Fu
Qing Wang
Jinhua Zuo
author_facet Lili Ma
Yanyan Zheng
Zhongjing Zhou
Zhiping Deng
Jinjuan Tan
Chunmei Bai
Anzhen Fu
Qing Wang
Jinhua Zuo
author_sort Lili Ma
collection DOAJ
description Abstract N4-acetylcytidine (ac4C) modification of mRNA has been shown to be present in plant RNAs, but its regulatory function in plant remains largely unexplored. In this study, we investigated the differentially expressed mRNAs, lncRNAs and acetylation modifications of mRNAs in tomato fruits from both genotypes. By comparing wild-type (AC) tomato and the ethylene receptor-mutant (Nr) tomato from mature green (MG) to six days after the breaker (Br6) stage, we identified differences in numerous key genes related to fruit ripening and observed the corresponding lncRNAs positively regulated the target genes expression. At the post-transcriptional level, the acetylation level decreased and increased in AC and Nr tomatoes from MG to Br6 stage, respectively. The integrated analysis of RNA-seq and ac4C-seq data revealed the potential positive role of acetylation modification in regulating gene expression. Furthermore, we found differential acetylation modifications of certain transcripts (ACO, ETR, ERF, PG, CesA, β-Gal, GAD, AMY, and SUS) in AC and Nr fruits which may explain the differences in ethylene production, fruit texture, and flavor during their ripening processes. The present study provides new insights into the molecular mechanisms by which acetylation modification differentially regulates the ripening process of wild-type and mutant tomato fruits deficient in ethylene signaling. Graphical Abstract
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spelling doaj.art-15876a341fe54e2e84ffbe25911562ba2024-03-05T20:21:20ZengBMCMolecular Horticulture2730-94012024-02-014111710.1186/s43897-024-00082-7Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethyleneLili Ma0Yanyan Zheng1Zhongjing Zhou2Zhiping Deng3Jinjuan Tan4Chunmei Bai5Anzhen Fu6Qing Wang7Jinhua Zuo8Institute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing Key Laboratory of Fruits and Vegetable Storage and Processing, Key Laboratory of Vegetable Postharvest Processing of Ministry of Agriculture and Rural Areas, State Key Laboratory of Vegetable Biobreeding, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry ScienceInstitute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing Key Laboratory of Fruits and Vegetable Storage and Processing, Key Laboratory of Vegetable Postharvest Processing of Ministry of Agriculture and Rural Areas, State Key Laboratory of Vegetable Biobreeding, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry ScienceZhejiang Academy of Agricultural SciencesZhejiang Academy of Agricultural SciencesZhejiang Academy of Agricultural SciencesInstitute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing Key Laboratory of Fruits and Vegetable Storage and Processing, Key Laboratory of Vegetable Postharvest Processing of Ministry of Agriculture and Rural Areas, State Key Laboratory of Vegetable Biobreeding, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry ScienceSchool of Food and Health, Beijing Technology and Business University (BTBU)Institute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing Key Laboratory of Fruits and Vegetable Storage and Processing, Key Laboratory of Vegetable Postharvest Processing of Ministry of Agriculture and Rural Areas, State Key Laboratory of Vegetable Biobreeding, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry ScienceInstitute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing Key Laboratory of Fruits and Vegetable Storage and Processing, Key Laboratory of Vegetable Postharvest Processing of Ministry of Agriculture and Rural Areas, State Key Laboratory of Vegetable Biobreeding, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry ScienceAbstract N4-acetylcytidine (ac4C) modification of mRNA has been shown to be present in plant RNAs, but its regulatory function in plant remains largely unexplored. In this study, we investigated the differentially expressed mRNAs, lncRNAs and acetylation modifications of mRNAs in tomato fruits from both genotypes. By comparing wild-type (AC) tomato and the ethylene receptor-mutant (Nr) tomato from mature green (MG) to six days after the breaker (Br6) stage, we identified differences in numerous key genes related to fruit ripening and observed the corresponding lncRNAs positively regulated the target genes expression. At the post-transcriptional level, the acetylation level decreased and increased in AC and Nr tomatoes from MG to Br6 stage, respectively. The integrated analysis of RNA-seq and ac4C-seq data revealed the potential positive role of acetylation modification in regulating gene expression. Furthermore, we found differential acetylation modifications of certain transcripts (ACO, ETR, ERF, PG, CesA, β-Gal, GAD, AMY, and SUS) in AC and Nr fruits which may explain the differences in ethylene production, fruit texture, and flavor during their ripening processes. The present study provides new insights into the molecular mechanisms by which acetylation modification differentially regulates the ripening process of wild-type and mutant tomato fruits deficient in ethylene signaling. Graphical Abstracthttps://doi.org/10.1186/s43897-024-00082-7ac4C modificationTomatoEthyleneFruit ripeningmRNA
spellingShingle Lili Ma
Yanyan Zheng
Zhongjing Zhou
Zhiping Deng
Jinjuan Tan
Chunmei Bai
Anzhen Fu
Qing Wang
Jinhua Zuo
Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
Molecular Horticulture
ac4C modification
Tomato
Ethylene
Fruit ripening
mRNA
title Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
title_full Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
title_fullStr Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
title_full_unstemmed Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
title_short Dissection of mRNA ac4C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene
title_sort dissection of mrna ac4c acetylation modifications in ac and nr fruits insights into the regulation of fruit ripening by ethylene
topic ac4C modification
Tomato
Ethylene
Fruit ripening
mRNA
url https://doi.org/10.1186/s43897-024-00082-7
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