Conservation in Geographical Utilization of Distinct Nuclear Chromatin Architectures in the Vertebrate Retinas: A...

Light refraction by transparent eye tissues focuses object images on photoreceptor outer segments for visual perception. To enhance this light-focusing function, heterochromatin in the rods of nocturnal mammals adapts to organize into a central clump that acts as a miniature converging lens. However, whether and how the nuclear architectures of other retinal cells affect vision in vertebrates remains unknown. Here, we examine chromatin organization patterns in the zebrafish retina under transmission electron microscopy (TEM) and compare them with those of other vertebrates. In the outer vertebrate retinal cells, chromatin is segregated in various patterns into more refractive heterochromatin and less refractive euchromatin, which we now name collectively "dualchromatin." By contrast, in the inner retinal cells, chromatin adopts a uniform architecture with no clear distinction between heterochromatin and euchromatin observable under TEM; we thus name such chromatin "unichromatin." The unichromatic architecture in the "inverted" vertebrate retinas is neither conserved in the "everted" retinas of cephalopods and gastropods nor in non-visual sensory systems of vertebrates. By basic optics, we infer that heterogeneous dualchromatin may distort light more than homogeneous unichromatin. Considering that the dualchromatic nuclear architecture may facilitate gene expression better than unichromatin, we propose that the geographically differential utilization of unichromatin and dualchromatin in the vertebrate retinas is a compromising evolutionary visual adaptation to balance the conflicting demands on nuclear architectures imposed by transcriptomic fitness and optical clarity.