Robust 3D Modelling Reveals Spatiosyntenic Properties of Animal Genomes

Abstract

Animal genomes are organised into chromosomes that are remarkably conserved in their gene content, forming distinct evolutionary units (synteny). Using versatile chromosomal modelling we reconstruct three-dimensional topology of genomes of phylogenetically informative species spanning the animal tree of life. We apply 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 can identify evolutionary conserved three-dimensional networks at all syntenic scales, encompassed within our interaction spheres. Using this approach, we were able to reveal novel evolutionarily maintained interactors associated with many conserved local gene linkages, including the hox gene cluster. We thus present evidence for evolutionary constraints that are associated with three-, rather than just two-, dimensional animal genome organisation, which we term spatiosynteny. Spatiosyntenic approaches may become relevant in understanding the functionally behind the observed high conservation of animal chromosomes.

Keywords: 3D genome organization, evolution, spatial co-localization, synteny