Nuclear Architecture of Rod Photoreceptor Cells Adapts to Vision in Mammalian Evolution

Abstract

We show that the nuclear architecture of rod photoreceptor cells differs fundamentally in nocturnal and diurnal mammals. The rods of diurnal retinas possess the conventional architecture found in nearly all eukaryotic cells, with most heterochromatin situated at the nuclear periphery and euchromatin residing toward the nuclear interior. The rods of nocturnal retinas have a unique inverted pattern, where heterochromatin localizes in the nuclear center, whereas euchromatin, as well as nascent transcripts and splicing machinery, line the nuclear border. The inverted pattern forms by remodeling of the conventional one during terminal differentiation of rods. The inverted rod nuclei act as collecting lenses, and computer simulations indicate that columns of such nuclei channel light efficiently toward the light-sensing rod outer segments. Comparison of the two patterns suggests that the conventional architecture prevails in eukaryotic nuclei because it results in more flexible chromosome arrangements, facilitating positional regulation of nuclear functions.

Characterization and dynamics of pericentromere-associated domains in mice

“…2C). These signatures of pericentromere-associated regions are in agreement with previously published FISH and immunofluorescence data showing that chromocenters are surrounded by a halo of heterochromatic histone marks (Solovei et al 2009;Eberhart et al 2013). The gene repression in PADs is not mediated by Polycomb-group proteins, as the Polycomb-associated H3K27me3 mark is mostly associated with genes in nonPADs (Fig.…”

“…Pericentromeric satellite repeats from different chromosomes cluster together into nuclear landmark structures called chromocenters (Baccarini 1908), which in murine nuclei are easily visualized using fluorescent DNA dyes such as DAPI (4 ′ ,6-diamidino-2-phenylindole), due to their preference for megabase-long tandem arrays of A/T-dense "major" satellite repeats (Mayer et al 2005;Probst and Almouzni 2008). This clustering appears to be cell type-specific, with large variations in the number, size, and radial position of chromocenters (Mayer et al 2005;Solovei et al 2009). Differentiation is generally accompanied by increased clustering into fewer but larger chromocenters and their relocation to the nuclear periphery (Beil et al 2002;Weierich et al 2003;Mayer et al 2005;Wiblin et al 2005).…”

Müller cells separate between wavelengths to improve day vision with minimal effect upon night vision

“…For nocturnal species another mechanism has been suggested, in which inverted rod nuclei act as collecting lenses, directing light onto the rod's outer segments 31,32 .…”

“…2a). Therefore, the observer needs to change the green/red ratio in a manner that will increase the red at the expense of the green, leading to a reduction in the green/red ratio 31 .…”

Loss of neuronal 3D chromatin organization causes transcriptional and behavioural deficits related to serotonergic dysfunction

“…The interior of the eukaryotic cell nucleus is a highly organized 3D structure in which regions of the genome that are millions of bases apart, even belonging to different chromosomes, work together and define specialized substructures with dedicated functions 4,5 . Thus, in most interphase somatic cells, pericentromeric regions are organized in clusters referred to as chromocenters that consist of transcriptionally silent DNA and exhibit species-and cell type-specific features [6][7][8] .…”