Aromatic ring overlap affects excited-state properties of stacked nucleobases.

Photochemistry of nucleic acids has gained considerable attention because of their ability to undergo efficient charge transfer (CT) after absorption of UV light, which contributes to DNA damage and repair. Recent computational and experimental studies demonstrated that CT rates and yields of DNA and RNA oligomers are strongly dependent on their secondary structure and relative arrangements of the chromophores. However, molecular and electronic origins of these differences still remain largely obscure. Here, we explored how stacking interactions and aromatic ring overlap affect the energetics of different locally excited (LE) and charge transfer (CT) states, as well as electronic couplings between them. For this purpose, we developed a novel approach and metric to quantify the stacking overlap between neighbouring aromatic rings. Based on quantum chemical calculations performed for a stacked adenine-guanine dimer, we show how the minima of different electronically excited states correlate with the degree of aromatic ring overlap and our stacking score metric. In particular, we demonstrate that electronic coupling values between the LE and CT states are maximised whenever the aromatic subunits of stacked nucleobases are in perfect horizontal overlap. These correlations are preserved for more realistic nucleic acid fragments, such as different conformers of the AG RNA dinucleotide. Since the magnitude of electronic coupling has a strong effect on the electron transfer rate, our results rationalize varying CT rates and yields observed across different DNA and RNA secondary structures, adopting different relative arrangements of the chromophores. Finally, our stacking score approach can be applied to the interpretation of excited-state and ground state properties of any chemical systems containing stacked aromatic rings.