Our understanding of oxidative damage to double helical DNA and the design of DNA-based devices for molecular electronics is crucially dependent upon elucidation of the mechanism and dynamics of electron and hole transport in DNA. Electrons and holes can migrate from the locus of formation to trap sites, and such migration can occur through either a single-step "superexchange" mechanism or a multistep charge transport "hopping" mechanism. The rates of single-step charge separation and charge recombination processes are found to decrease rapidly with increasing transfer distances, whereas multistep hole transport processes are only weakly distance dependent. However, the dynamics of hole transport has not yet been directly determined. Here we report spectroscopic measurements of photoinduced electron transfer in synthetic DNA that yield rate constants of approximately 5 x 10(7) s(-1) and 5 x 10(6) s(-1), respectively, for the forward and return hole transport from a single guanine base to a double guanine base step across a single adenine. These rates are faster than processes leading to strand cleavage, such as the reaction of guanine cation radical with water, thus permitting holes to migrate over long distances in DNA. However, they are too slow to compete with charge recombination in contact ion pairs, a process which protects DNA from photochemical damage.

The driving force dependence of photoinduced electron-transfer dynamics in duplex DNA has been investigated for 16 synthetic DNA hairpins in which an acceptor chromophore serves as a linker connecting two complementary oligonucleotide arms containing a single donor nucleobase located either adjacent to the linker or separated from the linker by two unreactive base pairs. The rate constants for both charge separation and charge recombination processes have been determined by means of subpicosecond time-resolved transient absorption spectroscopy and the results analyzed using quantum mechanical Marcus theory. This analysis provides intimate details about electron-transfer processes in DNA including the distance dependence of the electronic coupling between the acceptor and nucleobase donor and the solvent and nuclear reorganization energies.

Electron transfer (ET) processes in DNA are of current interest because of their involvement in oxidative strand cleavage reactions and their relevance to the development of molecular electronics. Two mechanisms have been identified for ET in DNA, a single-step tunneling process and a multistep charge-hopping process. The dynamics of tunneling reactions depend on both the distance between the electron donor and acceptor and the nature of the molecular bridge separating the donor and acceptor. In the case of protein and alkane bridges, the distance dependence is not strongly dependent on the properties of the donor and acceptor. In contrast, we show here that the distance decay of DNA ET rates varies markedly with the energetics of the donor and acceptor relative to the bridge. Specifically, we find that an increase in the energy of the bridge states by 0.25 eV (1 eV ‫؍‬ 1.602 ؋ 10 ؊19 J) relative to the donor and acceptor energies for photochemical oxidation of nucleotides, without changing the reaction free energy, results in an increase in the characteristic exponential distance decay constant for the ET rates from 0.71 to 1.1 Å ؊1 . These results show that, in the small tunneling energy gap regime of DNA ET, the distance dependence is not universal; it varies strongly with the tunneling energy gap. These DNA ET reactions fill a ''missing link'' or transition regime between the large barrier (rapidly decaying) tunneling regime and the (slowly decaying) hopping regime in the general theory of bridge-mediated ET processes. E lectron transfer (ET) processes in which an electron donor and acceptor are separated by a molecular spacer or bridge (D-B-A systems) are encountered widely in biological systems (proteins and DNA; refs. 1-4) and molecular wires (5-7). The dynamics of such processes are known to depend, inter alia, on the length and nature of the bridge (8, 9). The dynamics of single-step photoinduced ET in D-B-A systems, a process referred to as tunneling, is generally found to display an exponential dependence on the D-A distance as described by Eq. 1,where k o is a temperature-dependent prefactor, r da is the D-A separation, and ␤ characterizes the steepness of the experimental distance dependence are observed for bridges consisting of conjugated polyenes (5, 12), which probably arise from delocalization of the donor and acceptor states onto the bridge. DNA systems apparently are unique in that a wide range of values of ␤ (0.1-1.5 Å Ϫ1 ) have been observed for similar duplex DNA bridge structures (13,14). The very smallest ␤ values for DNA ET may arise from an alternative ET mechanism, multistep hole hopping (15-18). The distance dependence of the reorganization energy may enhance some of the observed ␤ values (19). A question in DNA ET is how much the donor and acceptor energetics can influence the ␤ value by tuning the electronic coupling strength. By making donor-acceptor modifications that do not change the ETactivation free energies, we find that ␤ values can be changed by more than 50%. We interpret...

The dynamics of single-step hole transport processes have been investigated in a number of DNA conjugates possessing a stilbenedicarboxamide electron acceptor, a guanine primary donor, and several secondary donors. Rate constants for both forward and return hole transport between the primary and secondary donor are obtained from kinetic modeling of the nanosecond transient absorption decay profiles of the stilbene anion radical. The kinetic model requires that the hole be localized on either the primary or the secondary donor and not delocalized over both the primary and the secondary donor. Rate constants for hole transport are found to be dependent upon the identity of the secondary donor, the intervening bases, and the location of the secondary donor in the same strand as the primary donor or in the complementary strand. Rate constants for hole transport are much slower than those for the superexchange process used to inject the hole on the primary donor. This difference is attributed to the larger solvent reorganization energy for charge transport versus charge separation. The hole transport rate constants obtained in these experiments are consistent with experimental data for single-step hole transport from other transient absorption studies. Their relevance to long-distance hole migration over tens of base pairs remains to be determined. The forward and return hole transport rate constants provide equilibrium constants and free energies for hole transport equilibria. Secondary GG and GGG donors are found to form very shallow hole traps, whereas the nucleobase deazaguanine forms a relatively deep hole trap. This conclusion is in accord with selected strand cleavage data and thus appears to be representative of the behavior of holes in duplex DNA. Our results are discussed in the context of current theoretical models of hole transport in DNA.

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