Arabidopsis ACINUS is O-glycosylated andregulates transcription and alternative splicingof 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, Zhi-Yong Wang.
Nature Communication; (2021)12:945 | https://doi.org/10.1038/s41467-021-20929
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/AtPININdependent AS events are altered in the sec and spy mutants, demonstrating a function of Oglycosylation in regulating alternative RNA splicing.
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Figure 1: AtACINUS and AtPININ are genetically redundant. a Diagrams of the domain structures of AtACINUS and AtPININ. SAP: SAF-A/B, Acinus, and PIAS motif. RRM: RNA-recognition motif. RSB: RNPS1–SAP18 binding domain. G and F indicates the position of O-GlcNAcylation and Ofucosylation modifications, respectively. b The sequence alignment of the RSB domains of AtACINUS and AtPININ. Conserved amino acids are highlighted in green. c Diagrams of the AtACINUS and AtPININ (translation start at position 1) with T-DNA insertion sites in acinus-1, acinus-2, and pinin-1 mutants. d Plant morphologies of wild-type (WT), acinus-1, acinus-2, pinin-1, acinus-1 pinin-1, and acinus-2 pinin-1 grown on soil for 20 days. e Fiveweek-old WT, acinus-1, acinus-2, pinin-1, acinus-1 pinin-1, and acinus-2 pinin-1 plants grown under long day condition. Inset shows enlarged view of the acinus-1 pinin-1 and acinus-2 pinin-1 mutants. f Expression of either AtACINUS-GFP or YFP-AtPININ suppresses the growth defects in acinus-2 pinin-1 double mutant (ap).
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