The evolution of high-order genome architecture revealed from 1,000 species

Spatial genome organization plays a crucial regulatory role, but its evolutionary development remains unclear. Leveraging Hi-C data from 1,025 species, we trace the evolutionary trajectories of genome organization through 2 higher-order architectures, "global folding" (spatial organization of the karyotype) and "checkerboard" (spatial organization of chromatin compartments). Earlier unicellular life forms mostly displayed random genome configurations. Throughout the evolution of plants, global folding became and remained the prominent architecture. However, animals progressively developed more pronounced checkerboard architectures; these are also apparent during early embryogenesis, which suggests that they act as a conserved mechanism of gene regulation. In contrast, plants exhibit comparatively weaker checkerboard patterns and instead preferentially organize co-regulated genes into linear genomic clusters. Both strategies of gene arrangement reinforce the biological principle that "structure determines function": divergent evolutionary paths converge on architectural solutions that reflect gene regulatory requirements over time.