Gene-rich and gene-poor chromosomal regions have different locations in the interphase nuclei of cold-blooded vertebrates

Abstract

In situ hybridizations of single-copy GC-rich, gene-rich and GC-poor, gene-poor chicken DNA allowed us to localize the gene-rich and the gene-poor chromosomal regions in interphase nuclei of cold-blooded vertebrates. Our results showed that the gene-rich regions from amphibians (Rana esculenta) and reptiles (Podarcis sicula) occupy the more internal part of the nuclei, whereas the gene-poor regions occupy the periphery. This finding is similar to that previously reported in warm-blooded vertebrates, in spite of the lower GC levels of the gene-rich regions of cold-blooded vertebrates. This suggests that this similarity extends to chromatin structure, which is more open in the gene-rich regions of both mammals and birds and more compact in the gene-poor regions. In turn, this may explain why the compositional transition undergone by the genome at the emergence of homeothermy did not involve the entire ancestral genome but only a small part of it, and why it involved both coding and noncoding sequences. Indeed, the GC level increased only in that part of the genome that needed a thermodynamic stabilization, namely in the more open gene-rich chromatin of the nuclear interior, whereas the gene-poor chromatin of the periphery was stabilized by its own compact structure.

An isochore map of human chromosomes

“…We proposed that the increasing body temperature accompanying the emergence of homeothermy led to a need for a thermodynamic stabilization of DNA . At the transition between coldand warm-blooded vertebrates, GC-poor isochores did not undergo any significant compositional change because they were stabilized by their closed chromatin structures, whereas GC increases took place in the gene-rich genome regions that were characterized by an open chromatin structure (Federico et al 2006). In fact, the stabilization also concerned RNA and proteins (GC-rich codons favoring amino acids that lead to a higher thermal stability) Nishio et al 2003).…”

The radial arrangement of the human chromosome 7 in the lymphocyte cell nucleus is associated with chromosomal band gene density

“…In general, the H3 + and L1 + chromosomal bands are not contiguous along the metaphase chromosome, and are typically separated by the compositionally intermediate H3 -and L1 -bands IHGSC 2004). This type of chromosome organization is highly conserved evolutionarily, and has been described not only in mammalian and avian species (Saccone et al 1997;Andreozzi et al 2001;Federico et al 2004;, but also in reptiles and amphibians (Federico et al 2006). The non-contiguity, in a chromosome, of the GC-richest H3 + and the GC-poorest L1 + bands, emphasises the very different location in nuclei of these two types of band.…”

Three-dimensional positioning of genes in mouse cell nuclei

“…However, results from Bernardi and coworkers suggest that a high GC content may be an evolutionary consequence of internal localization rather than the other way round (Federico et al 2006): In warm-blooded vertebrates, GC-rich isochores of the genome were found in central areas of the nucleus (Bernardi 2000;Saccone et al 2002;Federico et al 2004Federico et al , 2005. Compared to cold-blooded vertebrates, warm-blooded vertebrates have an increased GC content in gene-rich regions of the genome, most likely to thermodynamically stabilize the structure of genes transcribed in many tissues by increasing the binding forces between the DNA single strands (Jabbari and Bernardi 2004).…”

“…Compared to cold-blooded vertebrates, warm-blooded vertebrates have an increased GC content in gene-rich regions of the genome, most likely to thermodynamically stabilize the structure of genes transcribed in many tissues by increasing the binding forces between the DNA single strands (Jabbari and Bernardi 2004). However, despite the absence of high GC content in cold-blooded vertebrates, when DNA probes of GC-rich, gene-rich sequences from chicken were hybridized to nuclei of a frog and a lizard, the homologous regions detected were found in central areas of the nuclei (Federico et al 2006). An increase in GC content in warm-blooded animals could confer a selective advantage particularly in genes which are expressed in many different cell types while a selective advantage may be lower or absent for genes which are functionally important only in one cell type such as the β-globin gene or the neighboring olfactory receptor genes (Bulger et al 1999).…”