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The spliceosome-associated protein CWC15 promotes miRNA biogenesis in Arabidopsis

Author

Listed:
  • Bangjun Zhou

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

  • Huihui Yu

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

  • Yong Xue

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

  • Mu Li

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

  • Chi Zhang

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

  • Bin Yu

    (University of Nebraska-Lincoln
    University of Nebraska-Lincoln)

Abstract

MicroRNAs (miRNAs) play a key role in regulating gene expression and their biogenesis is precisely controlled through modulating the activity of microprocessor. Here, we report that CWC15, a spliceosome-associated protein, acts as a positive regulator of miRNA biogenesis. CWC15 binds the promoters of genes encoding miRNAs (MIRs), promotes their activity, and increases the occupancy of DNA-dependent RNA polymerases at MIR promoters, suggesting that CWC15 positively regulates the transcription of primary miRNA transcripts (pri-miRNAs). In addition, CWC15 interacts with Serrate (SE) and HYL1, two key components of microprocessor, and is required for efficient pri-miRNA processing and the HYL1-pri-miRNA interaction. Moreover, CWC15 interacts with the 20 S proteasome and PRP4KA, facilitating SE phosphorylation by PRP4KA, and subsequent non-functional SE degradation by the 20 S proteasome. These data reveal that CWC15 ensures optimal miRNA biogenesis by maintaining proper SE levels and by modulating pri-miRNA levels. Taken together, this study uncovers the role of a conserved splicing-related protein in miRNA biogenesis.

Suggested Citation

  • Bangjun Zhou & Huihui Yu & Yong Xue & Mu Li & Chi Zhang & Bin Yu, 2024. "The spliceosome-associated protein CWC15 promotes miRNA biogenesis in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46676-z
    DOI: 10.1038/s41467-024-46676-z
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    References listed on IDEAS

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    1. Zhiye Wang & Zeyang Ma & Claudia Castillo-González & Di Sun & Yanjun Li & Bin Yu & Baoyu Zhao & Pingwei Li & Xiuren Zhang, 2018. "SWI2/SNF2 ATPase CHR2 remodels pri-miRNAs via Serrate to impede miRNA production," Nature, Nature, vol. 557(7706), pages 516-521, May.
    2. Qiang Cai & Chao Liang & Suikang Wang & Yingnan Hou & Lei Gao & Li Liu & Wenrong He & Wenbo Ma & Beixin Mo & Xuemei Chen, 2018. "The disease resistance protein SNC1 represses the biogenesis of microRNAs and phased siRNAs," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    3. Seok Keun Cho & Samir Ben Chaabane & Pratik Shah & Christian Peter Poulsen & Seong Wook Yang, 2014. "COP1 E3 ligase protects HYL1 to retain microRNA biogenesis," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    4. Zhengyi Zhang & Jingnan Pi & Dongling Zou & Xiaoshuang Wang & Jiayue Xu & Shan Yu & Ting Zhang & Feng Li & Xianxie Zhang & Hualu Zhao & Fang Wang & Dong Wang & Yanni Ma & Jia Yu, 2019. "microRNA arm-imbalance in part from complementary targets mediated decay promotes gastric cancer progression," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    5. Chao Liang & Qiang Cai & Fei Wang & Shaofang Li & Chenjiang You & Chi Xu & Lei Gao & Dechang Cao & Ting Lan & Bailong Zhang & Beixin Mo & Xuemei Chen, 2022. "Arabidopsis RBV is a conserved WD40 repeat protein that promotes microRNA biogenesis and ARGONAUTE1 loading," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. David Baulcombe, 2004. "RNA silencing in plants," Nature, Nature, vol. 431(7006), pages 356-363, September.
    7. Wojciech P. Galej & Max E. Wilkinson & Sebastian M. Fica & Chris Oubridge & Andrew J. Newman & Kiyoshi Nagai, 2016. "Cryo-EM structure of the spliceosome immediately after branching," Nature, Nature, vol. 537(7619), pages 197-201, September.
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