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Replisomes restrict SMC translocation in vivo

Author

Listed:
  • Qin Liao

    (Indiana University)

  • Hugo B. Brandão

    (Illumina Inc.)

  • Zhongqing Ren

    (Indiana University
    Memorial Sloan Kettering Cancer Center)

  • Xindan Wang

    (Indiana University)

Abstract

Structural maintenance of chromosomes (SMC) complexes organize genomes by extruding DNA loops, while replisomes duplicate entire chromosomes. These essential molecular machines must collide frequently in every cell cycle, yet how such collisions are resolved in vivo remains poorly understood. Taking advantage of the ability to load SMC complexes at defined sites in the Bacillus subtilis genome, we engineered head-on and head-to-tail collisions between SMC complexes and the replisome. Replisome progression was monitored by genome-wide marker frequency analysis, and SMC translocation was monitored by time-resolved ChIP-seq and Hi-C. We found that SMC complexes do not impede replisome progression. By contrast, replisomes restrict SMC translocation regardless of collision orientations. Combining experimental data with simulations, we determined that SMC complexes are blocked by the replisome and then released from the chromosome. Occasionally, SMC complexes can bypass the replisome and continue translocating. Our findings establish that the replisome is a barrier to SMC-mediated DNA-loop extrusion in vivo, with implications for processes such as chromosome segregation, DNA repair, and gene regulation that require dynamic chromosome organization in all organisms.

Suggested Citation

  • Qin Liao & Hugo B. Brandão & Zhongqing Ren & Xindan Wang, 2025. "Replisomes restrict SMC translocation in vivo," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-62596-y
    DOI: 10.1038/s41467-025-62596-y
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    References listed on IDEAS

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    1. Christian H. Haering & Ana-Maria Farcas & Prakash Arumugam & Jean Metson & Kim Nasmyth, 2008. "The cohesin ring concatenates sister DNA molecules," Nature, Nature, vol. 454(7202), pages 297-301, July.
    2. Kati Böhm & Giacomo Giacomelli & Andreas Schmidt & Axel Imhof & Romain Koszul & Martial Marbouty & Marc Bramkamp, 2020. "Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    3. Coline Arnould & Vincent Rocher & Anne-Laure Finoux & Thomas Clouaire & Kevin Li & Felix Zhou & Pierre Caron & Philippe. E. Mangeot & Emiliano P. Ricci & Raphaël Mourad & James E. Haber & Daan Noorder, 2021. "Loop extrusion as a mechanism for formation of DNA damage repair foci," Nature, Nature, vol. 590(7847), pages 660-665, February.
    4. Eugene Kim & Jacob Kerssemakers & Indra A. Shaltiel & Christian H. Haering & Cees Dekker, 2020. "DNA-loop extruding condensin complexes can traverse one another," Nature, Nature, vol. 579(7799), pages 438-442, March.
    5. Iain F. Davidson & Roman Barth & Maciej Zaczek & Jaco Torre & Wen Tang & Kota Nagasaka & Richard Janissen & Jacob Kerssemakers & Gordana Wutz & Cees Dekker & Jan-Michael Peters, 2023. "CTCF is a DNA-tension-dependent barrier to cohesin-mediated loop extrusion," Nature, Nature, vol. 616(7958), pages 822-827, April.
    6. Chen-Yu Wang & David Colognori & Hongjae Sunwoo & Danni Wang & Jeannie T. Lee, 2019. "PRC1 collaborates with SMCHD1 to fold the X-chromosome and spread Xist RNA between chromosome compartments," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
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