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

BACKGROUND: N(6)-methyladenosine (m(6)A) mRNA modification is essential for mammalian and plant viability. The U6 m(6)A methyltransferases in other species regulate S-adenosylmethionine (SAM) homeostasis through installing m(6)A in pre-mRNAs of SAM synthetases. However, U6 m(6)A methyltransferase has not been characterized in Arabidopsis and little is known about its role in regulating photomorphogenesis and flowering. RESULTS: Here we characterize that FIONA1 is an Arabidopsis U6 m(6)A methyltransferase that installs m(6)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(6)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(6)A motifs in vitro and in vivo. We further show that FIONA1 installs m(6)A in several phenotypic related transcripts, thereby affecting downstream mRNA stability and regulating phytochrome signaling and floral transition. CONCLUSION: FIONA1 is functional as a U6 m(6)A methyltransferase in Arabidopsis, distinct from mammalian METTL16 and worm METT-10. Our results demonstrate that FIONA1-mediated m(6)A post-transcriptional regulation is an autonomous regulator for flowering and phytochrome signaling-dependent photomorphogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02612-2.