O-glycosylation regulates plant developmental transitions downstream of miR156

The timing of plant developmental transitions is decisive for reproductive success and thus tightly regulated. The transition from juvenile to adult vegetative and later to the reproductive phase is controlled by an endogenous pathway regulated by miR156, targeting the SQUAMOSA PROMOTER BINDING PROTEIN (SBP/SPL) family of transcription factors. SPLs regulate a number of developmental processes, such as trichome formation, leaf shape and floral transition. Such complex regulatory pathways often involve post-translational modifications (PTMs), integrating a range of internal and external signals. One of these PTMs is O-glycosylation, the attachment of a single monosaccharide to serine or threonine of nuclear and cytoplasmic proteins, which is found on a number of very diverse proteins. O-GlcNAcylation is the most common type of cytosolic O-glycosylation, but in plants also O-fucose modification occurs. Here we show that mutants defective in the O-fucosyltransferase SPINDLY (SPY) show accelerated developmental transitions. Genetic analysis shows that this effect is independent of miR156 levels, but partly dependent on functional SPLs. In a phenotyping analysis, we found that SPY and SPLs also control leaf growth, as loss of function mutants showed defects in cell expansion, while SPL9 also regulates cell division in rosette leaves. Moreover, SPLs interact directly with SPY and are O-glycosylated. Our results show that O-glycosylation is involved at several steps in the regulation of developmental transitions and organ growth in Arabidopsis thaliana.