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Evolutionary consequences of nonrandom damage and repair of chromatin domains

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Summary

Some evolutionary consequences of different rates and trends in DNA damage and repair are explained. Different types of DNA damaging agents cause nonrandom lesions along the DNA. The type of DNA sequence motifs to be preferentially attacked depends upon the chemical or physical nature of the assaulting agent and the DNA base composition. Higher-order chromatin structure, the nonrandom nucleosome positioning along the DNA, the absence of nucleosomes from the promoter regions of active genes, curved DNA, the presence of sequence-specific binding proteins, and the torsional strain on the DNA induced by an increased transcriptional activity all are expected to affect rates of damage of individual genes. Furthermore, potential Z-DNA, H-DNA, slippage, and cruciform structures in the regulatory region of some genes or in other genomic loci induced by torsional strain on the DNA are more prone to modification by genotoxic agents. A specific actively transcribed gene may be preferentially damaged over nontranscribed genes only in specific cell types that maintain this gene in active chromatin fractions because of (1) its decondensed chromatin structure, (2) torsional strain in its DNA, (3) absence of nucleosomes from its regulatory region, and (4) altered nucleosome structure in its coding sequence due to the presence of modified histones and HMG proteins. The situation in this regard of germ cell lineages is, of course, the only one to intervene in evolution. Most lesions in DNA such as those caused by UV or DNA alkylating agents tend to diminish the GC content of genomes. Thus, DNA sequences not bound by selective constraints, such as pseudogenes, will show an increase in their AT content during evolution as evidenced by experimental observations.

On the other hand, transcriptionally active parts may be repaired at rates higher than inactive parts of the genome, and proliferating cells may display higher repair activities than quiescent cells. This might arise from a tight coupling of the repair process with both transcription and replication, all these processes taking place on the nuclear matrix. Repair activities differ greatly among species, and there is a good correlation between life span and repair among mammals. It is predicted that genes that are transcriptionally active in germ-cell lineages have a lower mutation rate than bulk DNA, a circumstance that is expected to be reflected in evolution. Exception to this rule might be genes containing potential Z-DNA, H-DNA, or cruciform structures in their coding or regulatory regions that appear to be refractory to repair. This study supports the molecular clock hypothesis when applied to one gene within a group of related species and contends that evolutionary rates might vary between genes and gene segments not only as a result of differences in selective constraints but also as a result of differences in the rate of damage minus rate of repair among different segments of chromatin DNA.

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Abbreviations

MNNG:

N-methyl-N′-nitro-N-nitrosoguanidine

MNU:

N-methyl-N-nitrosourea

ENU:

N-ethyl-N-nitrosourea

HO-AAF:

N-hydroxy-2-acetylaminofluorene

DMBA:

7,12-dimethylbenz[a]anthracene

cis-DDP:

cis-diaminedichloroplatinum (II)

hsp:

heat shock protein

MHC:

major histocompatibility complex

CHO:

Chinese hamster ovary

ADA:

adenosine deaminase

DHFR:

dihydrofolate reductase

HPRT:

hypoxanthine (guanine) phosphoribosyltransferase

GPDH:

glyceraldehyde 3′ phosphate dehydrogenase

HMG:

high mobility group

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  1. Linus Pauling Institute of Science and Medicine and Institute of Molecular Medical Sciences, 440 Page Mill Road, 94306, Palo Alto, CA, USA

    Teni Boulikas

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Dedicated to Emile Zuckerkandl and Costas Kastritsis

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Boulikas, T. Evolutionary consequences of nonrandom damage and repair of chromatin domains. J Mol Evol 35, 156–180 (1992). https://doi.org/10.1007/BF00183227

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