FIONA1-mediated methylation of the 3'UTR of FLC affects FLC transcript levels and flowering in Arabidopsis

Bin Sun; Kaushal Kumar Bhati; Peizhe Song; Ashleigh Edwards; Louise Petri; Valdeko Kruusvee; Anko Blaakmeer; Ulla Dolde; Vandasue Rodrigues; Daniel Straub; Junbo Yang; Guifang Jia; Stephan Wenkel

doi:10.1371/journal.pgen.1010386

FIONA1-mediated methylation of the 3'UTR of FLC affects FLC transcript levels and flowering in Arabidopsis

PLoS Genet. 2022 Sep 27;18(9):e1010386. doi: 10.1371/journal.pgen.1010386. eCollection 2022 Sep.

Authors

Bin Sun^{1

2}, Kaushal Kumar Bhati^{1

2}, Peizhe Song³, Ashleigh Edwards^{1

2}, Louise Petri^{1

2}, Valdeko Kruusvee^{1

2}, Anko Blaakmeer^{1

2}, Ulla Dolde^{1

2}, Vandasue Rodrigues^{1

2}, Daniel Straub^{1

2

4}, Junbo Yang³, Guifang Jia³, Stephan Wenkel^{1

2

5}

Affiliations

¹ Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark.
² Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, Denmark.
³ Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University, Beijing, China.
⁴ Quantitative Biology Center (QBiC), University of Tübingen, Auf der Morgenstelle, Tübingen, Germany.
⁵ NovoCrops Center, Frederiksberg, Denmark.

Abstract

Adenosine bases of RNA can be transiently modified by the deposition of a methyl-group to form N6-methyladenosine (m6A). This adenosine-methylation is an ancient process and the enzymes involved are evolutionary highly conserved. A genetic screen designed to identify suppressors of late flowering transgenic Arabidopsis plants overexpressing the miP1a microProtein yielded a new allele of the FIONA1 (FIO1) m6A-methyltransferase. To characterize the early flowering phenotype of fio1 mutant plants we employed an integrative approach of mRNA-seq, Nanopore direct RNA-sequencing and meRIP-seq to identify differentially expressed transcripts as well as differentially methylated RNAs. We provide evidence that FIO1 is the elusive methyltransferase responsible for the 3'-end methylation of the FLOWERING LOCUS C (FLC) transcript. Furthermore, our genetic and biochemical data suggest that 3'-methylation stabilizes FLC mRNAs and non-methylated FLC is a target for rapid degradation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

3' Untranslated Regions / genetics
Adenosine / genetics
Adenosine / metabolism
Arabidopsis Proteins* / metabolism
Arabidopsis* / metabolism
Flowers / genetics
Flowers / metabolism
Gene Expression Regulation, Plant
Histones / genetics
MADS Domain Proteins / genetics
MADS Domain Proteins / metabolism
Methylation
Methyltransferases / genetics
Plants, Genetically Modified / genetics
Plants, Genetically Modified / metabolism
RNA, Messenger / genetics
RNA, Messenger / metabolism

Substances

3' Untranslated Regions
Arabidopsis Proteins
Histones
MADS Domain Proteins
RNA, Messenger
Methyltransferases
Adenosine

Grants and funding

We acknowledge funding through NovoCrops Centre (Novo Nordisk Foundation project number 2019OC53580 to S. W.), the Independent Research Fund Denmark (0136‐00015B and 0135‐00014B to S. W.), the Novo Nordisk Foundation (NNF18OC0034226 and NNF20OC0061440 to S. W.), and the funding of DataPLANT (NFDI 7/1 – 42077441) as part of the German National Research Data Infrastructure funded by the Deutsche Forschungsgemeinschaft (DFG – German Research Foundation). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.