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We use a combination of database analysis and quantum chemical studies to investigate the role of cis and trans Hoogsteen:Hoogsteen (H:H) base pairs and associated higher-order structures in RNA. We add three new examples to the list of previously identified base-pair combinations belonging to these families and, in addition to contextual classification and characterization of their structural and energetic features, we compare their interbase interaction energies and propensities toward participation in triplets and quartets. We find that some base pairs, which are nonplanar in their isolated minimum energy geometries, attain planarity and stability upon triplet formation. A:A H:H trans is the most frequent H:H combination in RNA structures. This base pair occurs at many distinct positions in known rRNA structures, where it helps in the interaction of ribosomal domains in the 50S subunit. It is also present as a part of tertiary interaction in tRNA structures. Although quantum chemical studies suggest an intrinsically nonplanar geometry for this base pair in isolated form, it has the tendency to attain planar geometry in RNA crystal structures by forming higher-order tertiary interactions or in the presence of additional base-phosphate interactions. The tendency of this base pair to form such additional interactions may be helpful in bringing together different segments of RNA, thus making it suitable for the role of facilitator for RNA folding. This also explains the high occurrence frequency of this base pair among all H:H interactions.

On the role of Hoogsteen:Hoogsteen interactions in RNA: Ab initio investigations of structures and energies