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

Abstract

ABSTRACTThe establishment of organ symmetry during multicellular development is a fundamental process shared by most living organisms. Here, we investigated how twoO-glycosyltransferases ofArabidopsis 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 vivoandin vitroby attachingO-fucose andO-linked-β-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 kinasePINOID(PID) gene locus to promote transcriptional repression. Our findings reveal a previously unrecognized mechanism forO-GlcNAc andO-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.