The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA.

Abstract

Plant development requires coordination among complex signaling networks to enhance the plant's adaptation to changing environments. DELLAs, transcription regulators originally identified as repressors of phytohormone gibberellin signaling, play a central role in integrating multiple signaling activities via direct protein interactions with key transcription factors. Here, we found that DELLA is mono-O-fucosylated by the novel O-fucosyltransferase SPINDLY (SPY) in Arabidopsis thaliana. O-fucosylation activates DELLA by promoting its interaction with key regulators in brassinosteroid- and light-signaling pathways, including BRASSINAZOLE-RESISTANT1 (BZR1), PHYTOCHROME-INTERACTING-FACTOR3 (PIF3) and PIF4. Moreover, spy mutants displayed elevated responses to gibberellin and brassinosteroid, 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 may have broader importance because SPY orthologs are conserved in prokaryotes and eukaryotes, thus suggesting that intracellular O-fucosylation may regulate a wide range of biological processes in diverse organisms.

Department

Description

Provenance

Citation

Published Version (Please cite this version)

10.1038/nchembio.2320

Publication Info

Zentella, Rodolfo, Ning Sui, Benjamin Barnhill, Wen-Ping Hsieh, Jianhong Hu, Jeffrey Shabanowitz, Michael Boyce, Neil E Olszewski, et al. (2017). The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA. Nat Chem Biol, 13(5). pp. 479–485. 10.1038/nchembio.2320 Retrieved from https://hdl.handle.net/10161/15816.

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Scholars@Duke

Boyce

Michael Scott Boyce

Associate Professor of Biochemistry

The Boyce Lab studies mammalian cell signaling through protein glycosylation. For the latest news, project information and publications from our group, please visit our web site at http://www.boycelab.org or follow us on Twitter at https://twitter.com/BoyceLab.

Zhou

Pei Zhou

Professor of Biochemistry

The Zhou lab focuses on the elucidation of the structure and dynamics of protein–protein and protein–ligand interactions and their functions in various cellular processes. Our current efforts are directed at enzymes and protein complexes involved in bacterial membrane biosynthesis, translesion DNA synthesis, co-transcriptional regulation, and host-pathogen interactions. Our investigations of these important cellular machineries have led to the development of novel antibiotics and cancer therapeutics, as well as the establishment of new biotechnology adventures.

 

The Zhou lab integrates a variety of biochemical and biophysical tools, including NMR, X-ray crystallography, cryo-EM, and enzymology. The lab has played a major role in the development and application of innovative NMR technologies, including high-resolution, high-dimensional spectral reconstruction techniques.

Sun

Tai-ping Sun

Professor of Biology

The diterpenoid phytohormone gibberellin (GA) plays pivotal roles in regulating growth and development throughout the life cycle of higher plants.  Mutations affecting GA biosynthesis or GA response were the key to control plant stature in wheat and rice that led to dramatically increased grain yield and contributed greatly to the success of the ‘Green Revolution’ in the 1960s.  By multi-faceted approaches using the reference plant Arabidopsis, my lab has made major breakthroughs in elucidating the sites and regulatory mechanisms of GA biosynthesis, and the conserved molecular events of GA perception and the early GA signaling pathway.  We identified the nuclear transcriptional regulators DELLA proteins, which function as master growth repressors by inhibiting all aspects of GA responses.  Binding of GA to its nuclear receptor GID1 enhances the GID1-DELLA interaction, which in turn leads to the rapid proteolysis of DELLA through the ubiquitin-proteasome pathway, and allows transcriptional reprogramming of GA-responsive genes.  We and other researchers further showed that GA-GID1-DELLA is a key regulatory module that controls plant growth by integrating internal developmental cues, and external biotic and abiotic signals (light, cold, salt and pathogen stresses).  DELLA proteins play a central role in these processes via direct protein-protein interactions with key transcription factors.  Our recent studies using genetic and physiological analyses together with chemical biology methods indicate that DELLA’s binding affinity to interacting proteins are oppositely regulated by two novel O-linked glycosylations on specific Ser/Thr residues: O-linked N-acetylglucosamine (O-GlcNAc) modification reduces DELLA activity, whereas O-fucosylation enhances DELLA activity.  We are investigating the global functions of O-GlcNAcylation and O-fucosylation in regulating plant development.


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