FIONA1‐Mediated m⁶A Modification Regulates the Floral Transition in Arabidopsis

Abstract

N6‐methyladenosine (m6A) mRNA modification represents the most widespread form of internal modifications in eukaryotic mRNAs. In the model plant Arabidopsis thaliana, those known methyltransferases mainly deposit m6A at their target transcripts near the stop codon or in the 3′ untranslated region. Here, it is reported that FIONA1 (FIO1), a human METTL16 ortholog, acts as a hitherto unknown m6A methyltransferase that determines m6A modifications at over 2000 Arabidopsis transcripts predominantly in the coding region. Mutants of FIO1 show a decrease in global m6A mRNA methylation levels and an early‐flowering phenotype. Nanopore direct RNA sequencing reveals that FIO1 is required for establishing appropriate levels of m6A preferentially in the coding sequences of a subset of protein‐coding transcripts, which is associated with changes in transcript abundance and alternative polyadenylation. It is further demonstrated that FIO1‐mediated m6A methylation determines the mRNA abundance of a central flowering integrator SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and its upstream regulators, thus preventing premature flowering. The findings reveal that FIO1 acts as a unique m6A methyltransferase that mainly modifies the coding regions of transcripts, which underlies the key developmental transition from vegetative to reproductive growth in plants.

m6A modification of U6 snRNA modulates usage of two major classes of pre-mRNA 5’ splice site

“…In contrast, we identified significant depletion of U6 snRNA in the anti-m 6 A immunopurified RNA from fio1-1, fio1-3 and fio1-4 alleles (Figure 3B-C). These data are consistent with recent reports (Wang et al, 2022; Xu et al, 2022) indicating that Arabidopsis U6 snRNA is m 6 A-modified at the conserved position of the AC m6 A GA box and that this modification requires active FIO1.…”

“…This screen identified an early flowering mutant disrupting the gene encoding the Arabidopsis METTL16 orthologue, FIONA1 (FIO1) (Kim et al, 2008). We show that FIO1 is required for m 6 A modification of U6 snRNA, consistent with recent reports confirming this conserved function (Wang et al, 2022; Xu et al, 2022). We reveal the impact of FIO1 on MAF2 splicing and global patterns of gene expression.…”

“…It is also possible that changes in patterns of gene expression caused by loss of FIO1 function perturb the canonical targeting of m 6 A in some transcripts by the METTL3-like writer complex. A combination of these phenomena, and different analytical approaches, might account for recent contrasting reports on FIO1-dependent mRNA methylation (Sun et al, 2022; Wang et al, 2022; Xu et al, 2022).…”

Light, chromatin, action: nuclear events regulating light signaling in Arabidopsis

“…As for chromatin modifications, RNA methylation is deposited by ‘writers’ (RNA methyltransferases), removed by ‘erasers’ (RNA demethylases) and recognized by ‘readers’ (Liang et al ., 2020). Two m 6 A writers have been identified in plants, a methyltransferase complex composed of at least five proteins, namely mRNA ADENOSINE METHYLASE (MTA; ortholog of METTL3 in animals), METHYLTRANSFERASE B (MTB; ortholog of METTL14), FKBP12 INTERACTING PROTEIN 37 (FIP37; ortholog of WTAP), VIRILIZER (ortholog of WIRMA) and HAKAI (Yue et al ., 2019), that is responsible for the majority of mRNA methylation, and FIONA1 that deposits m 6 A at U6 snRNAs and at a subset of mRNAs (Sun et al ., 2022; Wang et al ., 2022; Xu et al ., 2022). Both writers have been associated with plant light signaling and light regulation of circadian clock entrainment (Kim et al ., 2008; Parker et al ., 2020; X. Wang et al ., 2021).…”

“…With regards to the second m 6 A writer, FIONA1, was first identified by a causative mutation in an Arabidopsis EMS genetic screen for early flowering (Kim et al ., 2008), but its molecular function as an RNA methyltransferase has emerged only recently (Sun et al ., 2022; Wang et al ., 2022; Xu et al ., 2022). In this seminal study, FIONA1 was reported to extend the period length of the expression of central oscillator genes including CIRCADIAN CLOCK ASSOCIATED 1 ( CCA1 ), LATE ELONGATED HYPOCOTYL ( LHY ) and TOC1 , and to increase mRNA levels of key flowering regulatory genes CONSTANS ( CO ) and FLOWERING LOCUS T ( FT ; Kim et al ., 2008).…”