<p>Hallmarks of multicellular eukaryotic genome organization are chromosome territories, compartments, and loop-extrusion-mediated structures, including TADs. However, these have mainly been observed in model organisms, and most eukaryotes remain unexplored. Using Hi-C in the silkworm <i>Bombyx mori</i> we discover a novel chromatin folding structure, compartment S, which is “secluded” from the rest of the chromosome. This compartment exhibits loop extrusion features and a unique genetic and epigenetic landscape, and it localizes towards the periphery of chromosome territories. While euchromatin and heterochromatin display preferential compartmental contacts, S domains are remarkably devoid of contacts with other regions, including with other S domains. In polymer simulations, this contact pattern can only be explained by high loop extrusion activity within compartment S, combined with low extrusion elsewhere throughout the genome. This proposed targeting of loop extrusion is a novel phenomenon, not observed in vertebrate models, but we speculate may extend to more organisms, such as other insects. Overall, our study underscores how evolutionarily conserved mechanisms—compartmentalization and loop extrusion—can be repurposed to create new 3D genome architectures.</p>

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Unique territorial and compartmental organization of chromosomes in the holocentric silkworm

  • José Gil Jr,
  • Emily Navarrete,
  • Clio Hockens,
  • Neil Chowdhury,
  • Sameer Abraham,
  • Gaétan Cornilleau,
  • Elissa P Lei,
  • Julien Mozziconacci,
  • Edward J Banigan,
  • Leah F Rosin,
  • Leonid A Mirny,
  • Héloïse Muller,
  • Ines Anna Drinnenberg

摘要

Hallmarks of multicellular eukaryotic genome organization are chromosome territories, compartments, and loop-extrusion-mediated structures, including TADs. However, these have mainly been observed in model organisms, and most eukaryotes remain unexplored. Using Hi-C in the silkworm Bombyx mori we discover a novel chromatin folding structure, compartment S, which is “secluded” from the rest of the chromosome. This compartment exhibits loop extrusion features and a unique genetic and epigenetic landscape, and it localizes towards the periphery of chromosome territories. While euchromatin and heterochromatin display preferential compartmental contacts, S domains are remarkably devoid of contacts with other regions, including with other S domains. In polymer simulations, this contact pattern can only be explained by high loop extrusion activity within compartment S, combined with low extrusion elsewhere throughout the genome. This proposed targeting of loop extrusion is a novel phenomenon, not observed in vertebrate models, but we speculate may extend to more organisms, such as other insects. Overall, our study underscores how evolutionarily conserved mechanisms—compartmentalization and loop extrusion—can be repurposed to create new 3D genome architectures.