O-linked-β-N-Acetylglucosamine (O-GlcNAc) and O-fucose are two sugar-based post-translational modifications (PTMs) whose mechanistic role in plant signalling and transcriptional regulation is still largely unknown. Here, we investigated how two O-glycosyltransferase enzymes of Arabidopsis thaliana, SPINDLY (SPY) and SECRET AGENT (SEC) promote the activity of the bHLH transcription factor SPATULA (SPT), during morphogenesis of the plant female reproductive organ apex, the style. SPY and SEC modify N-terminal residues of SPT in vivo and in vitro by attaching O-fucose and O-GlcNAc, respectively. This post-translational regulation does not impact SPT homo- and hetero-dimerisation events, although it enhances the affinity of SPT for the kinase PINOID (PID) gene locus and its transcriptional repression. Our findings offer the first mechanistic example of the effect of O-GlcNAc and O-fucose on the activity of a plant transcription factor and reveal a previously unrecognized roles for SEC and SPY in orchestrating style elongation and shape.