show Abstracthide AbstractGenome organization in diverse eukaryotes follows conserved principles including the formation of chromosome territories (CT), chromatin compartments, and TADs. Here, we describe the 3D architecture of holocentric chromosomes in the silkworm Bombyx mori. At the genome-wide scale, B. mori chromosomes are highly territorial lacking any visible trans contact pattern. At the chromosomal scale, B. mori chromosomes segregate into three chromatin compartments: an active A and an inactive B as described in other eukaryotes, and a third type, X, with a unique contact pattern. Compartment X is strongly enriched for short-range interactions and depleted of long-range interactions, hosts a specific combination of genetic and epigenetic features and localizes towards the periphery of CT. Biophysical simulations reveal the necessity of the combined effects of affinity-based compartmentalization and activity-based loop extrusion to lead to the unique interaction patterns observed. Our analyses contribute to our understanding how chromosomes fold highlighting the evolutionary plasticity of 3D genome organization. Overall design: Hi-C and ChIP-seq and RNA-seq data from Bombyx mori p50 reference strain embryos post-diapause. ChIP-seq experimments are all performed in duplicates. Hi-C have been done at several embryonic time points: 2h, 24h and 48h after dipause release and on adults heads. RNA-seq has been perfomred at 24h after diapause release