Evolution of chromosome bands: Molecular ecology of noncoding DNA

Abstract

Giemsa dark bands, G-bands, are a derived chromatin character that evolved along the chromosomes of early chordates. They are facultative heterochromatin reflecting acquisition of a late replication mechanism to repress tissue-specific genes. Subsequently, R-bands, the primitive chromatin state, became directionally GC rich as evidenced by Q-banding of mammalian and avian chromosomes. Contrary to predictions from the neutral mutation theory, noncoding DNA is positionally constrained along the banding pattern with short interspersed repeats in R-bands and long interspersed repeats in G-bands. Chromosomes seem dynamically stable: the banding pattern and gene arrangement along several human and murine autosomes has remained constant for 100 million years, whereas much of the noncoding DNA, especially retroposons, has changed. Several coding sequence attributes and probably mutation rates are determined more by where a gene lives than by what it does. R-band exons in homeotherms but not G-band exons have directionally acquired GC-rich wobble bases and the corresponding codon usage: CpG islands in mammals are specific to R-band exons, exons not facultatively heterochromatinized, and are independent of the tissue expression pattern of the gene. The dynamic organization of noncoding DNA suggests a feedback loop that could influence codon usage and stabilize the chromosome's chromatin pattern: DNA sequences determine affinities of----proteins that together form----a chromatin that modulates----rate constants for DNA modification that determine----DNA sequences. Theories of hierarchical selection and molecular ecology show how selection can act on Darwinian units of noncoding DNA at the genome level thus creating positionally constrained DNA and contributing minimal genetic load at the individual level.

cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids

“…This conclusion is incompatible with previous observations using chromosome banding studies (Holmquist 1989) and density gradient centrifugation (Thiery et al 1976;Hughes et al 2002), which reported the lower level of GC heterogeneity in the turtle genome. Apart from the problems in sensitivity of the above indirect methods, the effect of lineage-specific events such as expansion of repetitive elements with extreme GC-contents might reconcile this difference.…”

“…The existence of intra-genomic GC heterogeneity in reptiles has not been fully confirmed by chromosome banding studies (Holmquist 1989) and density gradient centrifugation (Thiery et al 1976;Hughes et al 2002). However, some recent studies at the nucleotide level suggest that GC heterogeneity exists in reptilian genomes, based on variations in GC-contents in exonic third positions (GC 3 ) and introns of a limited number of genes (Hughes et al 1999;Belle et al 2002;Hamada et al 2003).…”

Molecular cytotaxonomy of primates by chromosomal in situ suppression hybridization

“…1e). This may support the recent findings that R-bands contain more conserved DNA sequences than G-bands (for reviews, see Holmquist, 1989; Bickmore and Sumner, 1989). These data further confirm Ohno's hypothesis that the X chromosome has been highly conserved during mammalian evolution (Ohno, 1973).…”

Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution

“…S6. somes are (G+C)-rich, CpG-rich and gene-rich [102][103][104] , exhibit features that are correlated with transcriptionally active DNA [105][106][107][108][109][110] , and have structural counterparts in the (G+C)-rich mammalian chromosomal R-bands (Table 8). Our current analysis shows that the different size classes of chicken chromosomes exhibit a number of correlated attributes.…”