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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. [ABSTRACT FROM AUTHOR]

The Streptophyta include unicellular and multicellular charophyte green algae and land plants. Colonization of the terrestrial habitat by land plants is a major evolutionary event that has transformed the planet. So far, lack of genome information on unicellular charophyte algae hinders the understanding of the origin and the evolution from unicellular to multicellular life in Streptophyta. This work reports the high‐quality reference genome and transcriptome of Mesostigma viride, a single‐celled charophyte alga with a position at the base of Streptophyta. There are abundant segmental duplications and transposable elements in M. viride, which contribute to a relatively large genome with high gene content compared to other algae and early diverging land plants. This work identifies the origin of genetic tools that multicellular Streptophyta have inherited and key genetic innovations required for the evolution of land plants from unicellular aquatic ancestors. The findings shed light on the age‐old questions of the evolution of multicellularity and the origin of land plants. [ABSTRACT FROM AUTHOR]