Relative roles of primary sequence and (G + C)% in determining the hierarchy of frequencies of complementary trinucleotide pairs in DNAs of different species

Abstract

To an approximation Chargaff's rule (%A = %T; %G = %C) applies to single-stranded DNA. In long sequences, not only complementary bases but also complementary oligonucleotides are present in approximately equal frequencies. This applies to all species studied. However, species usually differ in base composition. With the goal of understanding the evolutionary forces involved, I have compared the frequencies of trinucleotides in long sequences and their shuffled counterparts. Among the 32 complementary trinucleotide pairs there is a hierarchy of frequencies which is influenced both by base composition (not affected by shuffling the order of the bases) and by base order (affected by shuffling). The influence of base order is greatest in DNA of 50% G + C and seems to reflects a more fundamental hierarchy of dinucleotide frequencies. Thus if TpA is at low frequency, all eight TpA-containing trinucleotides are at low frequency. Mammals and their viruses share similar hierarchies, with intra-and intergenomic differences being mainly associated with differences in base composition (percentage G + C). E. coli and, to a lesser extent, Drosophila melanogaster hierarchies differ from mammalian hierarchies; this is associated with differences both in base composition and in base order. It is proposed that Chargaff's rule applies to single-stranded DNA because there has been an evolutionary selection pressure favoring mutations that generate complementary oligonucleotides in close proximity, thus creating a potential to form stem-loops. These are dispersed throughout genomes and are rate-limiting in recombination. Differences in (G + C)% between species would impair interspecies recombination by interfering with stem-loop interactions.

Relationships Between Genomic G+C Content, RNA Secondary Structures, and Optimal Growth Temperature in Prokaryotes

“…In contrast, no relationship was detected between genomic G+C content and T opt for prokaryotes. Forsdyke (1995a) suggested that the rough equalities between C and G (respectively, A and T) contents in single-stranded DNA are the result of selection pressure favoring the evolution of numerous secondary structures in bacterial genomes. If such structures actually exist, the G+C content of genomic sequences should behave similarly to the G+C content of tRNA and rRNA with respect to temperature.…”

“…Any deviations from PR2 would therefore be the result of deviation from the ideal no-strand-bias conditions, and these deviations are indeed correlated with the replication origin in E. coli, B. subtilis, Haemophilus influenzae (Lobry 1996a), and Mycoplasma genitalium (Lobry 1996b). The second interpretation is that PR2 is the result of a ''selection pressure favoring mutations that generate complementary oligonucleotides in close proximity, thus creating a potential to form stem-loops'' (Forsdyke 1995a). According to this hypothesis, deviations from PR2 are deviations from the ideal case, where the whole genome is involved in secondary structures.…”

Reciprocal relationship between stem-loop potential and substitution density in retroviral quasispecies under positive Darwinian selection

“…Thus the low frequency of the dinucleotide TpA seems to be universal. The dinucleotide CpG is in low frequency in many taxa but in high frequency in most bacteria (Nussinov 1994;Forsdyke 1995d). However, base order is predominantly a local "strategy," influencing both codons and stem-loop stability.…”

“…In this respect retroviral gehomes seem to offer a tractable model system for addressing general aspects of the speciation problem. Mechanisms by which percentage G + C differences might affect stem-loops and inhibit recombination are discussed elsewhere (Forsdyke 1995d). The importance of (G + C)% compatibility for recombination is emphasized by the observation that the high (G + C)% HTLV-1 genome is excluded from low (G + C)% sectors of the host genome (Zoubak et al 1994).…”

Sense in antisense?

“…Thus, it is possible that the divergence may be ascribed, in part, to "TpA pressure," which is a "known" but not well understood pressure (Nussinov 1984;Alff-Steinberger 1987;Barrai et al 1991). TpA pressure affects all codons of general forms NTA and TAN (Forsdyke 1995d).…”