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Spontaneous Mutagenesis
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Watson and Crick originally suggested that mutation could occur spontaneously during DNA replication if pairing errors occurred. If a base of the DNA underwent a proton shift into one of its rare tautomeric forms (tautomeric shift) during the replication process, an inappropriate pairing of bases would occur. Normally, adenine and cytosine are in the amino (NH2) form. Their tautomeric shifts are to the imino (NH) form. Similarly, guanine and thymine go from a keto (C O) form to an enol (COH) form ( g. 12.14). Table 12.4 shows the new
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Figure 12.14 Normal and tautomeric forms of DNA bases. Adenine and cytosine can exist in the
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amino, or the rare imino, forms; guanine and thymine can exist in the keto, or rare enol, forms.
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Tamarin: Principles of Genetics, Seventh Edition
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III. Molecular Genetics
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12. DNA: Its Mutation, Repair, and Recombination
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Mutation
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Table 12.4 Pairing Relationships of DNA Bases in
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the Normal and Tautomeric Forms
In Normal State Pairs with T A C G In Tautomeric State Pairs with C G T A
Base A T G C
base pairings that would occur following tautomeric shifts of the DNA bases. Figure 12.15 illustrates the molecular structure of one of these tautomeric pairings. During DNA replication, a tautomeric shift in either the incoming base (substrate transition) or the base already in the strand (template transition) results in mispairing. The mispairing will be permanent and result in a new base pair after an additional round of DNA replication. The original strand is unchanged ( g. 12.16). In the example in gure 12.16, the replacement of one base pair maintains the same purine-pyrimidine relationship: AT is replaced by GC and GC by AT. In both examples, a purine-pyrimidine combination is replaced by a purine-pyrimidine combination. (Or, more speci cally, a purine replaces another purine: guanine replaces
Template transition tautomerization of adenine in the template
Cytosine Substrate transition tautomerization of incoming adenine Figure 12.16 Tautomeric shifts result in transition mutations.
Adenine (amino)
The tautomerization can occur in the template base or in the substrate base. Tautomeric shifts are shown in red; the resulting transition in blue. The transition shows up after a second generation of DNA replication.
Cytosine
Adenine (amino) Figure 12.15 Tautomeric forms of adenine. In the common
amino form, adenine does not base-pair with cytosine; in the tautomeric imino form, it can.
adenine in the rst example and adenine replaces guanine in the second.) The mutation is referred to as a transition mutation: a purine (or pyrimidine) replaces another purine (or pyrimidine) through a transitional state involving a tautomeric shift. When a purine replaces a pyrimidine or vice versa, it is referred to as a transversion mutation. Transversions may arise by a combination of two events, a tautomerization and a base rotation. (We saw base rotations in the formation of Z DNA in chapter 9.) For example, an AT base pair can be converted to a TA base pair (a transversion) by an intermediate AA pairing
Tamarin: Principles of Genetics, Seventh Edition
III. Molecular Genetics
12. DNA: Its Mutation, Repair, and Recombination
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Twelve
DNA: Its Mutation, Repair, and Recombination
( g. 12.17). Adenine can pair with adenine if one of the bases undergoes a tautomeric shift while the other rotates about its base-sugar (glycosidic) bond ( g. 12.18). The normal con guration of the base is referred to as the anti con guration; the rotated form is the syn con guration. Since we now believe that as many as 10% of bases
Figure 12.17 A model for transversion mutagenesis. An AT
base pair can be converted to a TA base pair (a transversion) by way of an intermediate AA base pair. One of the red bases is in the rare tautomeric form, while the other is in the syn con guration. After a second round of DNA replication, one DNA duplex will have a transversion at that point (blue).
may be in the syn con guration at any moment, the transversion mutagenesis rate should be about 10% of the transition mutagenesis rate, a value not inconsistent with current information. Some base-pair mutations can have serious results. If guanine undergoes an oxidation to 8-oxoguanine ( g. 12.19), it pairs with adenine. A GC base pair is converted to a TA base pair through an 8-oxoguanineadenine intermediate. This transversion has been found to be common in cancers. Since 1953, when Watson and Crick rst described the structure of DNA, tautomerization has been accepted as the obvious source of most transition mutations. However, recent structural data has cast some doubt on this assumption. X-ray crystallography and nuclear magnetic resonance (NMR) studies indicate that both bases in transition mismatches may be in their normal forms. Other mechanisms, similar to wobble base pairing (see chapter 11), may be responsible for most transition mutations. These studies also indicate that some transversions result from direct purine-purine or pyrimidine-pyrimidine base pairing during DNA synthesis. Much work needs to be done to clarify the nature of spontaneous mutagenesis.
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