The FvABF3-FvALKBH10B-FvSEP3 Cascade Regulates Fruit Ripening in Strawberry

Overview

Journal Nat Commun

Specialty Biology

Date 2024 Dec 31

PMID 39738062

Authors

Renkun Tang

Xiaoyu Duan

Leilei Zhou

Guangtong Gao

Jinying Liu

Yuying Wang

Xingfeng Shao

Guozheng Qin

Affiliations

Soon will be listed here.

Abstract

Fruit ripening is a highly-orchestrated process that requires the fine-tuning and precise control of gene expression, which is mainly governed by phytohormones, epigenetic modifiers, and transcription factors. How these intrinsic regulators coordinately modulate the ripening remains elusive. Here we report the identification and characterization of FvALKBH10B as an N-methyladenosine (mA) RNA demethylase necessary for the normal ripening of strawberry (Fragaria vesca) fruit. FvALKBH10B is induced by phytohormone abscisic acid (ABA), and ABA-Responsive Element Binding Factor 3 (FvABF3), a master regulator in ABA signaling, is responsible for this activation. FvALKBH10B mutation leads to a delay in fruit ripening and causes global mA hypermethylation of 1859 genes. Further analyses show that FvALKBH10B positively modulates the mRNA stability of SEPALLATA3 (FvSEP3) encoding a transcription factor via mA demethylation. In turn, FvSEP3 targets numerous ripening-related genes including those associated with biosynthesis of ABA and anthocyanin and regulates their expression. Our findings uncover an FvABF3-FvALKBH10B-FvSEP3 cascade in controlling fruit ripening in strawberry and provide insights into the complex regulatory networks involved in this process.

References

Lee K, Liu K, Kim E, Medina-Puche L, Dong H, Di M . The m6A reader ECT1 drives mRNA sequestration to dampen salicylic acid-dependent stress responses in Arabidopsis. Plant Cell. 2023; 36(3):746-763. PMC: 10896288. DOI: 10.1093/plcell/koad300. View

Scutenaire J, Deragon J, Jean V, Benhamed M, Raynaud C, Favory J . The YTH Domain Protein ECT2 Is an mA Reader Required for Normal Trichome Branching in Arabidopsis. Plant Cell. 2018; 30(5):986-1005. PMC: 6002185. DOI: 10.1105/tpc.17.00854. View

Dominissini D, Moshitch-Moshkovitz S, Salmon-Divon M, Amariglio N, Rechavi G . Transcriptome-wide mapping of N(6)-methyladenosine by m(6)A-seq based on immunocapturing and massively parallel sequencing. Nat Protoc. 2013; 8(1):176-89. DOI: 10.1038/nprot.2012.148. View

Lei R, Qiao W, Hu F, Jiang H, Zhu S . A simple and effective method to encapsulate tobacco mesophyll protoplasts to maintain cell viability. MethodsX. 2015; 2:24-32. PMC: 4487327. DOI: 10.1016/j.mex.2014.11.004. View

Du Y, Hou G, Zhang H, Dou J, He J, Guo Y . SUMOylation of the m6A-RNA methyltransferase METTL3 modulates its function. Nucleic Acids Res. 2018; 46(10):5195-5208. PMC: 6007514. DOI: 10.1093/nar/gky156. View

Chen T, Qin G, Tian S . Regulatory network of fruit ripening: current understanding and future challenges. New Phytol. 2020; 228(4):1219-1226. DOI: 10.1111/nph.16822. View

Huang W, Hu N, Xiao Z, Qiu Y, Yang Y, Yang J . A molecular framework of ethylene-mediated fruit growth and ripening processes in tomato. Plant Cell. 2022; 34(9):3280-3300. PMC: 9421474. DOI: 10.1093/plcell/koac146. View

Oosumi T, Gruszewski H, Blischak L, Baxter A, Wadl P, Shuman J . High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta. 2005; 223(6):1219-30. DOI: 10.1007/s00425-005-0170-3. View

Wang X, Jiang B, Gu L, Chen Y, Mora M, Zhu M . A photoregulatory mechanism of the circadian clock in Arabidopsis. Nat Plants. 2021; 7(10):1397-1408. DOI: 10.1038/s41477-021-01002-z. View

10.

Wang C, Yang J, Song P, Zhang W, Lu Q, Yu Q . FIONA1 is an RNA N-methyladenosine methyltransferase affecting Arabidopsis photomorphogenesis and flowering. Genome Biol. 2022; 23(1):40. PMC: 8802475. DOI: 10.1186/s13059-022-02612-2. View

11.

Wang X, Lu Z, Gomez A, Hon G, Yue Y, Han D . N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2013; 505(7481):117-20. PMC: 3877715. DOI: 10.1038/nature12730. View

12.

Gutzat R, Rembart K, Nussbaumer T, Hofmann F, Pisupati R, Bradamante G . Arabidopsis shoot stem cells display dynamic transcription and DNA methylation patterns. EMBO J. 2020; 39(20):e103667. PMC: 7560203. DOI: 10.15252/embj.2019103667. View

13.

Shao Y, Wong C, Shen L, Yu H . N-methyladenosine modification underlies messenger RNA metabolism and plant development. Curr Opin Plant Biol. 2021; 63:102047. DOI: 10.1016/j.pbi.2021.102047. View

14.

Wei L, Song P, Wang Y, Lu Z, Tang Q, Yu Q . The mA Reader ECT2 Controls Trichome Morphology by Affecting mRNA Stability in Arabidopsis. Plant Cell. 2018; 30(5):968-985. PMC: 6002187. DOI: 10.1105/tpc.17.00934. View

15.

Jia H, Jiu S, Zhang C, Wang C, Tariq P, Liu Z . Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol J. 2016; 14(10):2045-65. PMC: 5043491. DOI: 10.1111/pbi.12563. View

16.

Seymour G, Ostergaard L, Chapman N, Knapp S, Martin C . Fruit development and ripening. Annu Rev Plant Biol. 2013; 64:219-41. DOI: 10.1146/annurev-arplant-050312-120057. View

17.

Fan W, Wang L, Lei Z, Li H, Chu J, Yan M . mA RNA demethylase AtALKBH9B promotes mobilization of a heat-activated long terminal repeat retrotransposon in . Sci Adv. 2023; 9(48):eadf3292. PMC: 10686560. DOI: 10.1126/sciadv.adf3292. View

18.

Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S . In vitro reconstitution of an abscisic acid signalling pathway. Nature. 2009; 462(7273):660-4. PMC: 2803041. DOI: 10.1038/nature08599. View

19.

Shen L, Liang Z, Gu X, Chen Y, Teo Z, Hou X . N(6)-Methyladenosine RNA Modification Regulates Shoot Stem Cell Fate in Arabidopsis. Dev Cell. 2016; 38(2):186-200. PMC: 6364302. DOI: 10.1016/j.devcel.2016.06.008. View

20.

Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K . Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci U S A. 2006; 103(6):1988-93. PMC: 1413621. DOI: 10.1073/pnas.0505667103. View