Post-translational modification of SPATULA by SECRET AGENT and SPINDLY promotes organ symmetry transition at the gynoecium apex

Abstract

The establishment of organ symmetry during multicellular development is a fundamental process shared by most living organisms. Here, we investigated how two O-glycosyltransferases of Arabidopsis thaliana, SPINDLY (SPY) and SECRET AGENT (SEC) synergistically promote a rare bilateral-to-radial symmetry transition during patterning of the plant reproductive organ, the gynoecium. SPY and SEC modify N-terminal residues of the bHLH transcription factor SPATULA (SPT) in vivo and in vitro by attaching O-fucose and O-linked-{beta}-N-Acetylglucosamine (O-GlcNAc), to promote style development. This post-translational regulation does not impact SPT homo- and hetero-dimerisation events with INDEHISCENT (IND) and HECATE 1 (HEC1), although it enhances the affinity of SPT for the kinase PINOID (PID) gene locus to promote transcriptional repression. Our findings reveal a previously unrecognized mechanism for O-GlcNAc and O-fucose post-translational decorations in controlling style development and offer the first molecular example of a synergistic role for SEC and SPY in plant post-embryonic organ patterning.