The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA

Plant development requires coordination among complex signaling networks to enhance plant’s adaptation to changing environments. The transcription regulators DELLAs, originally identified as repressors of phytohormone gibberellin (GA) signaling, play a central role in integrating multiple signaling activities via direct protein interactions with key transcription factors. Here, we showed that DELLA was mono-O-fucosylated by a novel O-fucosyltransferase SPINDLY (SPY) in Arabidopsis thaliana. O-fucosylation activates DELLA by promoting its interaction with key regulators in brassinosteroid (BR)- and light-signaling pathways, including BRASSINAZOLE-RESISTANT1 (BZR1), PHYTOCHROME-INTERACTING-FACTOR3 (PIF3), and PIF4. Consistently, spy mutants displayed elevated responses to GA and BR, and increased expression of common target genes of DELLAs, BZR1 and PIFs. Our study revealed that SPY-dependent protein O-fucosylation plays a key role in regulating plant development. This finding has broader importance as SPY orthologs are conserved from prokaryotes to eukaryotes, suggesting that intracellular O-fucosylation may regulate a wide range of biological processes in diverse organisms.