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

Author summaryPlants constantly measure environmental parameters such as temperature, light-quality, -quantity and -duration, as well as other parameters to adjust their growth and development. The transition to flowering is a crucial transition during plant development because it impacts the number of fertile offspring a plant can produce. Thus, this transition is under tight control by various transcription factors and epigenetic mechanisms. In a genetic screen for early flowering mutants, we identified the gene encoding the FIONA1 methyltransferase to act as a repressor of flowering. Investigation of the changes of the transcriptome and m(6)A-RNA-methylome revealed a large number of differentially expressed genes and methylated RNAs. Among these RNAs is the also the mRNA of the floral repressor FLOWERING LOCUS C that shows loss of m(6)A methylation in the 3'UTR that causes destabilization of the FLC transcript. Adenosine bases of RNA can be transiently modified by the deposition of a methyl-group to form N-6-methyladenosine (m(6)A). 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) m(6)A-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.

Automated summary

This study discovered the inhibitory role of FIONA1 methyltransferase in the flowering process of plants. Various differentially expressed genes and methylated RNAs, including RNA molecules that regulate flowering, were identified. Through the analysis of transcripts and methylated RNAs, the researchers found the mechanism of FIO1 methyltransferase in methylation of the FLOWERING LOCUS C transcript, further revealing the molecular mechanisms of flowering regulation.