FIONA1 is an RNA N 6 -methyladenosine methyltransferase affecting Arabidopsis photomorphogenesis and flowering

N -methyladenosine (m A) mRNA modification is essential for mammalian and plant viability. The U6 m A methyltransferases in other species regulate S-adenosylmethionine (SAM) homeostasis through installing m A in pre-mRNAs of SAM synthetases. However, U6 m A methyltransferase has not been characterized in Arabidopsis and little is known about its role in regulating photomorphogenesis and flowering. Here we characterize that FIONA1 is an Arabidopsis U6 m A methyltransferase that installs m A in U6 snRNA and a small subset of poly(A) RNA. Disruption of FIONA1 leads to phytochrome signaling-dependent hypocotyl elongation and photoperiod-independent early flowering. Distinct from mammalian METTL16 and worm METT-10, FIONA1 neither installs m A in the mRNAs of Arabidopsis SAM synthetases nor affects their transcript expression levels under normal or high SAM conditions. We confirm that FIONA1 can methylate plant mRNA m A motifs in vitro and in vivo. We further show that FIONA1 installs m A in several phenotypic related transcripts, thereby affecting downstream mRNA stability and regulating phytochrome signaling and floral transition. FIONA1 is functional as a U6 m A methyltransferase in Arabidopsis, distinct from mammalian METTL16 and worm METT-10. Our results demonstrate that FIONA1-mediated m A post-transcriptional regulation is an autonomous regulator for flowering and phytochrome signaling-dependent photomorphogenesis.