Arabidopsis ACINUS is O-glycosylated and regulates transcription and alternative splicing of regulators of reproductive transitions

Yang Bi, Zhiping Deng, Weimin Ni, Ruben Shrestha, Dasha Savage, Thomas Hartwig, Sunita Patil, Su Hyun Hong, Zhenzhen Zhang, Juan A. Oses-Prieto, Kathy H. Li, Peter H. Quail, Alma L. Burlingame, Shou-Ling Xu () and Zhi-Yong Wang ()
Additional contact information
Yang Bi: Carnegie Institution for Science
Zhiping Deng: Carnegie Institution for Science
Weimin Ni: United States Department of Agriculture/Agriculture Research Service
Ruben Shrestha: Carnegie Institution for Science
Dasha Savage: Carnegie Institution for Science
Thomas Hartwig: Carnegie Institution for Science
Sunita Patil: Carnegie Institution for Science
Su Hyun Hong: Carnegie Institution for Science
Zhenzhen Zhang: Carnegie Institution for Science
Juan A. Oses-Prieto: University of California, San Francisco
Kathy H. Li: University of California, San Francisco
Peter H. Quail: United States Department of Agriculture/Agriculture Research Service
Alma L. Burlingame: University of California, San Francisco
Shou-Ling Xu: Carnegie Institution for Science
Zhi-Yong Wang: Carnegie Institution for Science

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract O-GlcNAc modification plays important roles in metabolic regulation of cellular status. Two homologs of O-GlcNAc transferase, SECRET AGENT (SEC) and SPINDLY (SPY), which have O-GlcNAc and O-fucosyl transferase activities, respectively, are essential in Arabidopsis but have largely unknown cellular targets. Here we show that AtACINUS is O-GlcNAcylated and O-fucosylated and mediates regulation of transcription, alternative splicing (AS), and developmental transitions. Knocking-out both AtACINUS and its distant paralog AtPININ causes severe growth defects including dwarfism, delayed seed germination and flowering, and abscisic acid (ABA) hypersensitivity. Transcriptomic and protein-DNA/RNA interaction analyses demonstrate that AtACINUS represses transcription of the flowering repressor FLC and mediates AS of ABH1 and HAB1, two negative regulators of ABA signaling. Proteomic analyses show AtACINUS’s O-GlcNAcylation, O-fucosylation, and association with splicing factors, chromatin remodelers, and transcriptional regulators. Some AtACINUS/AtPININ-dependent AS events are altered in the sec and spy mutants, demonstrating a function of O-glycosylation in regulating alternative RNA splicing.

Date: 2021
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DOI: 10.1038/s41467-021-20929-7

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