Robust 3D modeling reveals spatiosyntenic properties of animal genomes

Animal genomes are organized into chromosomes that are remarkably conserved in their gene content, forming distinct evolutionary units (synteny). Using versatile chromosomal modeling, we infer three-dimensional topology of genomes from representative clades spanning the earliest animal diversification. We apply a partitioning approach using interaction spheres to compensate for varying quality of topological data. Using comparative genomics approaches, we test whether syntenic signal at gene pair, local, and whole chromosomal scale is reflected in the reconstructed spatial organization. We identify evolutionarily conserved three-dimensional networks at all syntenic scales revealing novel evolutionarily maintained interactors associated with known conserved local gene linkages (such as hox). We thus present evidence for evolutionary constraints that are associated with three-, rather than just two-, dimensional animal genome organization, which we term spatiosynteny. As more accurate topological data become available, together with validation approaches, spatiosynteny may become relevant in understanding the functionality behind the observed conservation of animal chromosomes.