IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46676-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46676-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46676-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    4. David Baulcombe, 2004. "RNA silencing in plants," Nature, Nature, vol. 431(7006), pages 356-363, September.
    5. 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.
    6. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Daai Zhang & Chengcheng Zhong & Neil A. Smith & Robert de Feyter & Ian K. Greaves & Steve M. Swain & Ren Zhang & Ming-Bo Wang, 2022. "Nucleotide mismatches prevent intrinsic self-silencing of hpRNA transgenes to enhance RNAi stability in plants," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Ahmed Moursy & Antoine Cléry & Stefan Gerhardy & Katharina M. Betz & Sanjana Rao & Jarosław Mazur & Sébastien Campagne & Irene Beusch & Malgorzata M. Duszczyk & Mark D. Robinson & Vikram Govind Panse , 2023. "RNA recognition by Npl3p reveals U2 snRNA-binding compatible with a chaperone role during splicing," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Si Liu & Meijuan Chen & Ruidong Li & Wan-Xiang Li & Amit Gal-On & Zhenyu Jia & Shou-Wei Ding, 2022. "Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Adeeb Rahman & Neeti Sanan-Mishra, 2024. "When an Intruder Comes Home: GM and GE Strategies to Combat Virus Infection in Plants," Agriculture, MDPI, vol. 14(2), pages 1-26, February.
    6. Salman Naveed & Sachin Rustgi, 2023. "Functional Characterization of Candidate Genes, Gohir.D05G103700 and Gohir.D12G153600 , Identified through Expression QTL Analysis Using Virus-Induced Gene Silencing in Upland Cotton ( Gossypium hirsu," Agriculture, MDPI, vol. 13(5), pages 1-12, May.
    7. Dong Zhang & Lulu Qiao & Xiaobo Lei & Xiaojing Dong & Yunguang Tong & Jianwei Wang & Zhiye Wang & Ruhong Zhou, 2023. "Mutagenesis and structural studies reveal the basis for the specific binding of SARS-CoV-2 SL3 RNA element with human TIA1 protein," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Jana Aupič & Jure Borišek & Sebastian M. Fica & Wojciech P. Galej & Alessandra Magistrato, 2023. "Monovalent metal ion binding promotes the first transesterification reaction in the spliceosome," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46676-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.