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

Abstract

Background: N6-methyladenosine (m6A) mRNA modification is essential for mammalian and plant viability. The U6 m6A methyltransferases in other species regulate S-adenosylmethionine (SAM) homeostasis through installing m6A in pre-mRNAs of SAM synthetases. However, U6 m6A 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 m6A methyltransferase that installs m6A 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 m6A 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 m6A motifs in vitro and in vivo. We further show that FIONA1 installs m6A in several phenotypic related transcripts, thereby affecting downstream mRNA stability and regulating phytochrome signaling and floral transition. Conclusion: FIONA1 is functional as a U6 m6A methyltransferase in Arabidopsis, distinct from mammalian METTL16 and worm METT-10. Our results demonstrate that FIONA1-mediated m6A post-transcriptional regulation is an autonomous regulator for flowering and phytochrome signaling-dependent photomorphogenesis.