IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51789-6.html
   My bibliography  Save this article

A repressive H3K36me2 reader mediates Polycomb silencing

Author

Listed:
  • Mengting Xu

    (Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University)

  • Qi Zhang

    (Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University)

  • Huanbin Shi

    (China National Rice Research Institute)

  • Zhongling Wu

    (Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University)

  • Wei Zhou

    (Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University)

  • Fucheng Lin

    (Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences)

  • Yanjun Kou

    (China National Rice Research Institute)

  • Zeng Tao

    (Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University)

Abstract

In animals, evolutionarily conserved Polycomb repressive complex 2 (PRC2) catalyzes histone H3 lysine 27 trimethylation (H3K27me3) and PRC1 functions in recruitment and transcriptional repression. However, the mechanisms underlying H3K27me3-mediated stable transcriptional silencing are largely unknown, as PRC1 subunits are poorly characterized in fungi. Here, we report that in the filamentous fungus Magnaporthe oryzae, the N-terminal chromodomain and C-terminal MRG domain of Eaf3 play key roles in facultative heterochromatin formation and transcriptional silencing. Eaf3 physically interacts with Ash1, Eed, and Sin3, encoding an H3K36 methyltransferase, the core subunit of PRC2, and a histone deacetylation co-suppressor, respectively. Eaf3 co-localizes with a set of repressive Ash1-H3K36me2 and H3K27me3 loci and mediates their transcriptional silencing. Furthermore, Eaf3 acts as a histone reader for the repressive H3K36me2 and H3K27me3 marks. Eaf3-occupied regions are associated with increased nucleosome occupancy, contributing to transcriptional silencing in M. oryzae. Together, these findings reveal that Eaf3 is a repressive H3K36me2 reader and plays a vital role in Polycomb gene silencing and the formation of facultative heterochromatin in fungi.

Suggested Citation

  • Mengting Xu & Qi Zhang & Huanbin Shi & Zhongling Wu & Wei Zhou & Fucheng Lin & Yanjun Kou & Zeng Tao, 2024. "A repressive H3K36me2 reader mediates Polycomb silencing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51789-6
    DOI: 10.1038/s41467-024-51789-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51789-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51789-6?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. Haipeng Guan & Pei Wang & Pei Zhang & Chun Ruan & Yutian Ou & Bo Peng & Xiangdong Zheng & Jianlin Lei & Bing Li & Chuangye Yan & Haitao Li, 2023. "Diverse modes of H3K36me3-guided nucleosomal deacetylation by Rpd3S," Nature, Nature, vol. 620(7974), pages 669-675, August.
    2. Chang Huang & Fu Yang & Zhuqiang Zhang & Jing Zhang & Gaihong Cai & Lin Li & Yong Zheng & She Chen & Rongwen Xi & Bing Zhu, 2017. "Mrg15 stimulates Ash1 H3K36 methyltransferase activity and facilitates Ash1 Trithorax group protein function in Drosophila," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    3. Giacomo Cavalli & Edith Heard, 2019. "Advances in epigenetics link genetics to the environment and disease," Nature, Nature, vol. 571(7766), pages 489-499, July.
    4. Shuiming Qian & Xinchen Lv & Ray N. Scheid & Li Lu & Zhenlin Yang & Wei Chen & Rui Liu & Melissa D. Boersma & John M. Denu & Xuehua Zhong & Jiamu Du, 2018. "Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    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. Qiang Zhang & Sai Ma & Zhengzhi Liu & Bohan Zhu & Zirui Zhou & Gaoshan Li & J. Javier Meana & Javier González-Maeso & Chang Lu, 2023. "Droplet-based bisulfite sequencing for high-throughput profiling of single-cell DNA methylomes," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Kimberly Matheson & Ann Seymour & Jyllenna Landry & Katelyn Ventura & Emily Arsenault & Hymie Anisman, 2022. "Canada’s Colonial Genocide of Indigenous Peoples: A Review of the Psychosocial and Neurobiological Processes Linking Trauma and Intergenerational Outcomes," IJERPH, MDPI, vol. 19(11), pages 1-28, May.
    3. van Dijk, Ingrid K. & Nilsson, Therese & Quaranta, Luciana, 2024. "Disease exposure in infancy affects women's reproductive outcomes and offspring health in southern Sweden 1905–2000," Social Science & Medicine, Elsevier, vol. 347(C).
    4. Xiaoyan Wei & Angelos Rigopoulos & Matthias Lienhard & Sophie Pöhle-Kronawitter & Georgios Kotsaris & Julia Franke & Nikolaus Berndt & Joy Orezimena Mejedo & Hao Wu & Stefan Börno & Bernd Timmermann &, 2024. "Neurofibromin 1 controls metabolic balance and Notch-dependent quiescence of murine juvenile myogenic progenitors," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Raúl F. Pérez & Patricia Tezanos & Alfonso Peñarroya & Alejandro González-Ramón & Rocío G. Urdinguio & Javier Gancedo-Verdejo & Juan Ramón Tejedor & Pablo Santamarina-Ojeda & Juan José Alba-Linares & , 2024. "A multiomic atlas of the aging hippocampus reveals molecular changes in response to environmental enrichment," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    6. Ming Wang & Zhenhui Zhong & Javier Gallego-Bartolomé & Suhua Feng & Yuan-Hsin Shih & Mukun Liu & Jessica Zhou & John Curtis Richey & Charmaine Ng & Yasaman Jami-Alahmadi & James Wohlschlegel & Keqiang, 2023. "Arabidopsis TRB proteins function in H3K4me3 demethylation by recruiting JMJ14," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Léa Maitre & Mariona Bustamante & Carles Hernández-Ferrer & Denise Thiel & Chung-Ho E. Lau & Alexandros P. Siskos & Marta Vives-Usano & Carlos Ruiz-Arenas & Dolors Pelegrí-Sisó & Oliver Robinson & Dan, 2022. "Multi-omics signatures of the human early life exposome," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Linying Jia & Ao Cheng & Naqash Alam & Yuxuan Qian & Zeyao Ma & Honghao Ren & Rong Wang & Enqi Liu, 2021. "Global Trends in Atherosclerosis Research in the Epigenetics Field: Bibliometric and Visualization Studies," IJERPH, MDPI, vol. 18(24), pages 1-12, December.
    9. Suzanne Mavoa & Daniel Keevers & Stefan C. Kane & Melissa Wake & Rachel Tham & Kate Lycett & Yen Ting Wong & Katherine Chong, 2021. "Parental Preconception Exposures to Outdoor Neighbourhood Environments and Adverse Birth Outcomes: A Protocol for a Scoping Review and Evidence Map," IJERPH, MDPI, vol. 18(17), pages 1-10, August.
    10. Jacob Bergstedt & Sadoune Ait Kaci Azzou & Kristin Tsuo & Anthony Jaquaniello & Alejandra Urrutia & Maxime Rotival & David T. S. Lin & Julia L. MacIsaac & Michael S. Kobor & Matthew L. Albert & Darrag, 2022. "The immune factors driving DNA methylation variation in human blood," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    11. Andrea Baccarelli & Dana C. Dolinoy & Cheryl Lyn Walker, 2023. "A precision environmental health approach to prevention of human disease," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Angela Tung & Megan M. Sperry & Wesley Clawson & Ananya Pavuluri & Sydney Bulatao & Michelle Yue & Ramses Martinez Flores & Vaibhav P. Pai & Patrick McMillen & Franz Kuchling & Michael Levin, 2024. "Embryos assist morphogenesis of others through calcium and ATP signaling mechanisms in collective teratogen resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    13. Mattia Zaghi & Federica Banfi & Luca Massimino & Monica Volpin & Edoardo Bellini & Simone Brusco & Ivan Merelli & Cristiana Barone & Michela Bruni & Linda Bossini & Luigi Antonio Lamparelli & Laura Pi, 2023. "Balanced SET levels favor the correct enhancer repertoire during cell fate acquisition," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    14. Grégoire Vernaz & Milan Malinsky & Hannes Svardal & Mingliu Du & Alexandra M. Tyers & M. Emília Santos & Richard Durbin & Martin J. Genner & George F. Turner & Eric A. Miska, 2021. "Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    15. Mary V. Seeman, 2022. "Subjective Overview of Accelerated Aging in Schizophrenia," IJERPH, MDPI, vol. 20(1), pages 1-8, December.
    16. Xiaozhen Zhao & Yiming Wang & Bingqin Yuan & Hanxi Zhao & Yujie Wang & Zheng Tan & Zhiyuan Wang & Huijun Wu & Gang Li & Wei Song & Ravi Gupta & Kenichi Tsuda & Zhonghua Ma & Xuewen Gao & Qin Gu, 2024. "Temporally-coordinated bivalent histone modifications of BCG1 enable fungal invasion and immune evasion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    17. Lasse Pihlstrøm & Gemma Shireby & Hanneke Geut & Sandra Pilar Henriksen & Annemieke J. M. Rozemuller & Jon-Anders Tunold & Eilis Hannon & Paul Francis & Alan J. Thomas & Seth Love & Jonathan Mill & Wi, 2022. "Epigenome-wide association study of human frontal cortex identifies differential methylation in Lewy body pathology," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    18. Corina Maritz & Reihaneh Khaleghi & Michelle N. Yancoskie & Sarah Diethelm & Sonja Brülisauer & Natalia Santos Ferreira & Yang Jiang & Shana J. Sturla & Hanspeter Naegeli, 2023. "ASH1L-MRG15 methyltransferase deposits H3K4me3 and FACT for damage verification in nucleotide excision repair," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Johanna Beil & Juliane Perner & Lena Pfaller & Marie-Apolline Gérard & Alessandro Piaia & Arno Doelemeyer & Adi Wasserkrug Naor & Lori Martin & Aline Piequet & Valérie Dubost & Salah-Dine Chibout & Jo, 2023. "Unaltered hepatic wound healing response in male rats with ancestral liver injury," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Denny Vågerö & Agneta Cederström & Gerard J. Berg, 2022. "Food abundance in men before puberty predicts a range of cancers in grandsons," Nature Communications, Nature, vol. 13(1), pages 1-9, 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_s41467-024-51789-6. 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.