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.

SECRET AGENT O-GlcNAcylates hundreds of proteins involved in diverse cellular processes in Arabidopsis

“…Our comprehensive profiling of O-GlcNAc datasets has significantly expanded the number of overlapping substrates to 189, encompassing almost one-third of the detected targets. Remarkably, aside from their previously documented contrasting effects on the DELLA group (11, 40), recent findings illustrate that SEC and SPY collaboratively regulate style development through the bHLH transcription factor SPATULA (42). These new insights uncover novel roles for O-glycosylation and synergistic effects of these two sugar modifications.…”