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N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner

BACKGROUND: Epigenetic mark such as DNA methylation plays pivotal roles in regulating ripening of both climacteric and non-climacteric fruits. However, it remains unclear whether mRNA m(6)A methylation, which has been shown to regulate ripening of the tomato, a typical climacteric fruit, is function...

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Autores principales: Zhou, Leilei, Tang, Renkun, Li, Xiaojing, Tian, Shiping, Li, Bingbing, Qin, Guozheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8173835/
https://www.ncbi.nlm.nih.gov/pubmed/34078442
http://dx.doi.org/10.1186/s13059-021-02385-0
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author Zhou, Leilei
Tang, Renkun
Li, Xiaojing
Tian, Shiping
Li, Bingbing
Qin, Guozheng
author_facet Zhou, Leilei
Tang, Renkun
Li, Xiaojing
Tian, Shiping
Li, Bingbing
Qin, Guozheng
author_sort Zhou, Leilei
collection PubMed
description BACKGROUND: Epigenetic mark such as DNA methylation plays pivotal roles in regulating ripening of both climacteric and non-climacteric fruits. However, it remains unclear whether mRNA m(6)A methylation, which has been shown to regulate ripening of the tomato, a typical climacteric fruit, is functionally conserved for ripening control among different types of fruits. RESULTS: Here we show that m(6)A methylation displays a dramatic change at ripening onset of strawberry, a classical non-climacteric fruit. The m(6)A modification in coding sequence (CDS) regions appears to be ripening-specific and tends to stabilize the mRNAs, whereas m(6)A around the stop codons and within the 3′ untranslated regions is generally negatively correlated with the abundance of associated mRNAs. We identified thousands of transcripts with m(6)A hypermethylation in the CDS regions, including those of NCED5, ABAR, and AREB1 in the abscisic acid (ABA) biosynthesis and signaling pathway. We demonstrate that the methyltransferases MTA and MTB are indispensable for normal ripening of strawberry fruit, and MTA-mediated m(6)A modification promotes mRNA stability of NCED5 and AREB1, while facilitating translation of ABAR. CONCLUSION: Our findings uncover that m(6)A methylation regulates ripening of the non-climacteric strawberry fruit by targeting the ABA pathway, which is distinct from that in the climacteric tomato fruit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-021-02385-0.
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spelling pubmed-81738352021-06-03 N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner Zhou, Leilei Tang, Renkun Li, Xiaojing Tian, Shiping Li, Bingbing Qin, Guozheng Genome Biol Research BACKGROUND: Epigenetic mark such as DNA methylation plays pivotal roles in regulating ripening of both climacteric and non-climacteric fruits. However, it remains unclear whether mRNA m(6)A methylation, which has been shown to regulate ripening of the tomato, a typical climacteric fruit, is functionally conserved for ripening control among different types of fruits. RESULTS: Here we show that m(6)A methylation displays a dramatic change at ripening onset of strawberry, a classical non-climacteric fruit. The m(6)A modification in coding sequence (CDS) regions appears to be ripening-specific and tends to stabilize the mRNAs, whereas m(6)A around the stop codons and within the 3′ untranslated regions is generally negatively correlated with the abundance of associated mRNAs. We identified thousands of transcripts with m(6)A hypermethylation in the CDS regions, including those of NCED5, ABAR, and AREB1 in the abscisic acid (ABA) biosynthesis and signaling pathway. We demonstrate that the methyltransferases MTA and MTB are indispensable for normal ripening of strawberry fruit, and MTA-mediated m(6)A modification promotes mRNA stability of NCED5 and AREB1, while facilitating translation of ABAR. CONCLUSION: Our findings uncover that m(6)A methylation regulates ripening of the non-climacteric strawberry fruit by targeting the ABA pathway, which is distinct from that in the climacteric tomato fruit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-021-02385-0. BioMed Central 2021-06-03 /pmc/articles/PMC8173835/ /pubmed/34078442 http://dx.doi.org/10.1186/s13059-021-02385-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhou, Leilei
Tang, Renkun
Li, Xiaojing
Tian, Shiping
Li, Bingbing
Qin, Guozheng
N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title_full N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title_fullStr N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title_full_unstemmed N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title_short N(6)-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner
title_sort n(6)-methyladenosine rna modification regulates strawberry fruit ripening in an aba-dependent manner
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8173835/
https://www.ncbi.nlm.nih.gov/pubmed/34078442
http://dx.doi.org/10.1186/s13059-021-02385-0
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