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Aromaticity of nucleic acid bases

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Halina Szatylowicz, Olga A. Stasyuk, Miquel Solà, Tadeusz M. Krygowski

Published Online: Dec 14 2020

DOI: 10.1002/wcms.1509

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Abstract 3D shape and the resulting physicochemical properties of double‐helical DNA/RNA structures are determined not only by individual nucleobases, but also by their additive intermolecular interactions. Energetic contribution from aromatic π–π stacking to the stabilization of DNA/RNA is not small and sometimes even comparable to that from H‐bonding. The basis of the stacking interactions lies in the π‐electron structure of individual nucleobases, which can be described by various aromaticity indices. Heteroatoms and exocyclic functional groups make the electronic structure of nucleobases different from aromatic hydrocarbons. Consequently, the cyclic π‐electron delocalization is not the only factor responsible for the relative stability of their tautomers. This review puts the spotlight on interplay between aromaticity of purine and pyrimidine nucleobases and their tautomeric preferences, as well as on the effects of different noncovalent interactions (hydrogen bonding, metal ion coordination, and π–π stacking) on π‐electron delocalization of five‐ and six‐membered rings in individual nucleobases and their complexes. This article is categorized under: Structure and Mechanism > Molecular Structures Electronic Structure Theory > Density Functional Theory

Structures of expanded nucleobases (a) and comparison of the local aromaticity descriptors for the six‐membered ring of natural (red) and benzo‐fused (yellow) bases (b) (Adapted with permission from Reference 59. Copyright (2006) American Chemical Society)

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Tetramers of adenine with C8, N9 and C2 positions of substitution (X = NO₂, Cl, F, H, Me, NH₂) and structure of guanine quartet (G₄) with metal cations (Mⁿ⁺)

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NICS profiles along the axis through the center of adenine rings from −2 to +2 Å with a step of 0.1 Å for acenaphthylene‐adenine (Ace_A[1]) complex(Adapted with permission from Reference 97. Copyright (2016) Wiley)

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Possible coordination sites of alkali metal cations (M⁺ = Li⁺, Na⁺, K⁺) for AT and GC pairs

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Left: Schematic illustration of aromaticity‐modulated hydrogen bonding in Watson–Crick AT and GC pairs. Resonance structures with (4N + 2) π‐electrons are in red. Right: Plot of interaction energy (−ΔE, in kcal/mol) versus π‐conjugation gain (ΔDE_π) in the gas‐phase for 57 nucleobase pairs (Adapted from Reference 92 with permission from The Royal Society of Chemistry)

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Possible resonance forms of the guanine‐cytosine base pair

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Six most stable cytosine tautomers and the most stable isocytosine tautomer

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Structures of the most stable thymine tautomers and possible stabilizing bond dipole interactions

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Relationship between aromaticity index HOMA6 and relative energy of uracil, thymine, cytosine, and isocytosine tautomers. Blue circles, red diamonds and black crosses denote tautomers with high, medium and low aromaticity (Data taken from References 79 and 80)

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The most stable tautomers of uracil and intramolecular interactions in them

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The most stable tautomers of guanine

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Structures of most stable amino tautomers of adenine

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Left: Variability of HOMED values for tautomers of imidazole (a), 4‐aminopyrimidine (b), purine (c), and adenine (d) in the gas phase (red color) and in water solution (blue color). Right: Correlations between HOMED indices and relative energies of tautomers(Adapted from Reference 69 with permission from The Royal Society of Chemistry)

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Further Reading

Karas, LJ, Wu, C‐H, Das, R, Wu, JI‐C. Hydrogen bond design principles. WIREs Comput Mol Sci. 2020;10:e1477. https://doi.org/10.1002/wcms.1477
Schleyer, PR. Aromaticity. Chem Rev. 2001;101(5):1115–1566.
Schleyer, PR, editor. Delocalization‐pi and sigma. Chem Rev. 2005;105(10):3343–3947.
Shukla, MK, Leszczynski, J. Tautomerism in nucleic acid bases and base pairs: A brief overview. WIREs Comput Mol Sci. 2013;3:637–649.
Solà, M. Connecting and combining rules of aromaticity. Towards a unified theory of aromaticity. WIREs Comput Mol Sci. 2019;9:e1404.

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