IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48940-8.html
   My bibliography  Save this article

A conserved Pol II elongator SPT6L mediates Pol V transcription to regulate RNA-directed DNA methylation in Arabidopsis

Author

Listed:
  • Yujuan Liu

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    University of the Chinese Academy of Sciences)

  • Jie Shu

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    Guangzhou)

  • Zhi Zhang

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    University of the Chinese Academy of Sciences)

  • Ning Ding

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    School of Life Sciences, Lanzhou University)

  • Jinyuan Liu

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    University of the Chinese Academy of Sciences)

  • Jun Liu

    (Guangzhou)

  • Yuhai Cui

    (London Research and Development Centre
    Western University)

  • Changhu Wang

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    University of the Chinese Academy of Sciences)

  • Chen Chen

    (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    South China Botanical Garden, Chinese Academy of Sciences, Guangzhou
    University of the Chinese Academy of Sciences)

Abstract

In plants, the plant-specific RNA polymerase V (Pol V) transcripts non-coding RNAs and provides a docking platform for the association of accessory proteins in the RNA-directed DNA methylation (RdDM) pathway. Various components have been uncovered that are involved in the process of DNA methylation, but it is still not clear how the transcription of Pol V is regulated. Here, we report that the conserved RNA polymerase II (Pol II) elongator, SPT6L, binds to thousands of intergenic regions in a Pol II-independent manner. The intergenic enrichment of SPT6L, interestingly, co-occupies with the largest subunit of Pol V (NRPE1) and mutation of SPT6L leads to the reduction of DNA methylation but not Pol V enrichment. Furthermore, the association of SPT6L at Pol V loci is dependent on the Pol V associated factor, SPT5L, rather than the presence of Pol V, and the interaction between SPT6L and NRPE1 is compromised in spt5l. Finally, Pol V RIP-seq reveals that SPT6L is required to maintain the amount and length of Pol V transcripts. Our findings thus uncover the critical role of a Pol II conserved elongator in Pol V mediated DNA methylation and transcription, and shed light on the mutual regulation between Pol V and II in plants.

Suggested Citation

  • Yujuan Liu & Jie Shu & Zhi Zhang & Ning Ding & Jinyuan Liu & Jun Liu & Yuhai Cui & Changhu Wang & Chen Chen, 2024. "A conserved Pol II elongator SPT6L mediates Pol V transcription to regulate RNA-directed DNA methylation 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_s41467-024-48940-8
    DOI: 10.1038/s41467-024-48940-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48940-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48940-8?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. Li He & Huan Huang & Mariem Bradai & Cheng Zhao & Yin You & Jun Ma & Lun Zhao & Rosa Lozano-Durán & Jian-Kang Zhu, 2022. "DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Zhihuan Gao & Hai-Liang Liu & Lucia Daxinger & Olga Pontes & Xinjian He & Weiqiang Qian & Huixin Lin & Mingtang Xie & Zdravko J. Lorkovic & Shoudong Zhang & Daisuke Miki & Xiangqiang Zhan & Dominique , 2010. "An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation," Nature, Nature, vol. 465(7294), pages 106-109, May.
    3. Julie A. Law & Jiamu Du & Christopher J. Hale & Suhua Feng & Krzysztof Krajewski & Ana Marie S. Palanca & Brian D. Strahl & Dinshaw J. Patel & Steven E. Jacobsen, 2013. "Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1," Nature, Nature, vol. 498(7454), pages 385-389, June.
    4. Seychelle M. Vos & Lucas Farnung & Marc Boehning & Christoph Wigge & Andreas Linden & Henning Urlaub & Patrick Cramer, 2018. "Structure of activated transcription complex Pol II–DSIF–PAF–SPT6," Nature, Nature, vol. 560(7720), pages 607-612, August.
    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. Wojciech Barczak & Simon M. Carr & Geng Liu & Shonagh Munro & Annalisa Nicastri & Lian Ni Lee & Claire Hutchings & Nicola Ternette & Paul Klenerman & Alexander Kanapin & Anastasia Samsonova & Nicholas, 2023. "Long non-coding RNA-derived peptides are immunogenic and drive a potent anti-tumour response," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Xiaohe Lin & Junjie Yin & Yifan Wang & Jing Yao & Qingshun Q. Li & Vit Latzel & Oliver Bossdorf & Yuan-Ye Zhang, 2024. "Environment-induced heritable variations are common in Arabidopsis thaliana," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Yan Li & Qianmin Wang & Yanhui Xu & Ze Li, 2024. "Structures of co-transcriptional RNA capping enzymes on paused transcription complex," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Seina Ohe & Yuji Kubota & Kiyoshi Yamaguchi & Yusuke Takagi & Junichiro Nashimoto & Hiroko Kozuka-Hata & Masaaki Oyama & Yoichi Furukawa & Mutsuhiro Takekawa, 2022. "ERK-mediated NELF-A phosphorylation promotes transcription elongation of immediate-early genes by releasing promoter-proximal pausing of RNA polymerase II," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Roberto Bandiera & Rebecca E. Wagner & Thiago Britto-Borges & Christoph Dieterich & Sabine Dietmann & Susanne Bornelöv & Michaela Frye, 2021. "RN7SK small nuclear RNA controls bidirectional transcription of highly expressed gene pairs in skin," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Tatsuo Yanagisawa & Yuko Murayama & Haruhiko Ehara & Mie Goto & Mari Aoki & Shun-ichi Sekine, 2024. "Structural basis of eukaryotic transcription termination by the Rat1 exonuclease complex," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Michael DeBerardine & Gregory T. Booth & Philip P. Versluis & John T. Lis, 2023. "The NELF pausing checkpoint mediates the functional divergence of Cdk9," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Yinwen Zhang & Hosung Jang & Rui Xiao & Ioanna Kakoulidou & Robert S. Piecyk & Frank Johannes & Robert J. Schmitz, 2021. "Heterochromatin is a quantitative trait associated with spontaneous epiallele formation," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    9. Ida Shinder & Richard Hu & Hyun Joo Ji & Kuan-Hao Chao & Mihaela Pertea, 2023. "EASTR: Identifying and eliminating systematic alignment errors in multi-exon genes," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Emily G. Kaye & Kavyashree Basavaraju & Geoffrey M. Nelson & Helena D. Zomer & Debarun Roy & Irene Infancy Joseph & Reza Rajabi-Toustani & Huanyu Qiao & Karen Adelman & Prabhakara P. Reddi, 2024. "RNA polymerase II pausing is essential during spermatogenesis for appropriate gene expression and completion of meiosis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Lisa-Marie Appel & Vedran Franke & Melania Bruno & Irina Grishkovskaya & Aiste Kasiliauskaite & Tanja Kaufmann & Ursula E. Schoeberl & Martin G. Puchinger & Sebastian Kostrhon & Carmen Ebenwaldner & M, 2021. "PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    12. Annkatrin Bressin & Olga Jasnovidova & Mirjam Arnold & Elisabeth Altendorfer & Filip Trajkovski & Thomas A. Kratz & Joanna E. Handzlik & Denes Hnisz & Andreas Mayer, 2023. "High-sensitive nascent transcript sequencing reveals BRD4-specific control of widespread enhancer and target gene transcription," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Hong-Wei Zhang & Kun Huang & Zhan-Xi Gu & Xiao-Xian Wu & Jia-Wei Wang & Yu Zhang, 2023. "A cryo-EM structure of KTF1-bound polymerase V transcription elongation complex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    14. Abdallah Gaballa & Anneli Gebhardt-Wolf & Bastian Krenz & Greta Mattavelli & Mara John & Giacomo Cossa & Silvia Andreani & Christina Schülein-Völk & Francisco Montesinos & Raphael Vidal & Carolin Kast, 2024. "PAF1c links S-phase progression to immune evasion and MYC function in pancreatic carcinoma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Zsolt Karányi & Ágnes Mosolygó-L & Orsolya Feró & Adrienn Horváth & Beáta Boros-Oláh & Éva Nagy & Szabolcs Hetey & Imre Holb & Henrik Mihály Szaker & Márton Miskei & Tibor Csorba & Lóránt Székvölgyi, 2022. "NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    16. Zheng Li & Ming Wang & Zhenhui Zhong & Javier Gallego-Bartolomé & Suhua Feng & Yasaman Jami-Alahmadi & Xinyi Wang & James Wohlschlegel & Sylvain Bischof & Jeff A. Long & Steven E. Jacobsen, 2023. "The MOM1 complex recruits the RdDM machinery via MORC6 to establish de novo DNA methylation," Nature Communications, Nature, vol. 14(1), pages 1-16, 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_s41467-024-48940-8. 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.