SPINDLY mediates O-fucosylation of hundreds of proteins and sugar-dependent growth in Arabidopsis

Yang Bi, Ruben Shrestha, Zhenzhen Zhang, Chuan-Chih Hsu, Andres V. Reyes, Sumudu Karunadasa, Peter R. Baker, Jason C. Maynard, Yang Liu, Amirmansoor Hakimi, Daniel Lopez-Ferrer, Tahmid Hassan, Robert J. Chalkley, Shou-Ling Xu*, Zhi-Yong Wang*

*Corresponding author for this work

Research output: Contribution to journalJournal articlepeer-review

6 Citations (Scopus)

Abstract

The recent discovery of SPINDLY (SPY)-catalyzed protein O-fucosylation revealed a novel mechanism for regulating nucleocytoplasmic protein functions in plants. Genetic evidence indicates the important roles of SPY in diverse developmental and physiological processes. However, the upstream signal controlling SPY activity and the downstream substrate proteins O-fucosylated by SPY remain largely unknown. Here, we demonstrated that SPY mediates sugar-dependent growth in Arabidopsis (Arabidopsis thaliana). We further identified hundreds of O-fucosylated proteins using lectin affinity chromatography followed by mass spectrometry. All the O-fucosylation events quantified in our proteomic analyses were undetectable or dramatically decreased in the spy mutants, and thus likely catalyzed by SPY. The O-fucosylome includes mostly nuclear and cytosolic proteins. Many O-fucosylated proteins function in essential cellular processes, phytohormone signaling, and developmental programs, consistent with the genetic functions of SPY. The O-fucosylome also includes many proteins modified by O-linked N-acetylglucosamine (O-GlcNAc) and by phosphorylation downstream of the target of rapamycin (TOR) kinase, revealing the convergence of these nutrient signaling pathways on key regulatory functions such as post-transcriptional/translational regulation and phytohormone responses. Our study identified numerous targets of SPY/O-fucosylation and potential nodes of crosstalk among sugar/nutrient signaling pathways, enabling future dissection of the signaling network that mediates sugar regulation of plant growth and development.

Original languageEnglish
Pages (from-to)1318-1333
Number of pages16
JournalPlant Cell
Volume35
Issue number5
Early online date6 Feb 2023
DOIs
Publication statusPublished - May 2023

Scopus Subject Areas

  • Plant Science

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