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Abstract
Tetraloop-receptor interactions are prevalent structural units in RNAs, and include the GAAA/11-nt and GNRA-minor groove interactions. In this study, we have compiled a set of 78 nonredundant loop-helix interactions from X-ray crystal structures, and examined them for the extent of their sequence and structural variation. Of the 78 interactions in the set, only four were classical GAAA/11-nt motifs, while over half (48) were GNRA-minor groove interactions. The GNRA-minor groove interactions were not a homogeneous set, but were divided into five subclasses. The most predominant subclass is characterized by two triple base pair interactions in the minor groove, flanked by two ribose zipper contacts. This geometry may be considered the “standard” GNRA-minor groove interaction, while the other four subclasses are alternative ways to form interfaces between a minor groove and tetraloop. The remaining 26 structures in the set of 78 have loops interacting with mostly idiosyncratic receptors. Among the entire set, a number of sequence-structure correlations can be identified, which may be used as initial hypotheses in predicting three-dimensional structures from primary sequences. Conversely, other sequence patterns are not predictive; for example, GAAA loop sequences and GG/CC receptors bind to each other with three distinct geometries. Finally, we observe an example of structural evolution in group II introns, in which loop-receptor motifs are substituted for each other while maintaining the larger three-dimensional geometry. Overall, the study gives a more complete view of RNA loop-helix interactions that exist in nature.
Highlights
Tetraloop-receptor interactions are common and well-studied organizers of RNA tertiary structure
The UNCG tetraloop forms an especially stable structure [2,3], with its closing nucleotides T1 and T4 forming a U-G base pair, and T2 and T3 extending on either side of the backbone (Figure 1A). (In this manuscript the four tetraloop positions are denoted T1, T2, T3 and T4)
The GNRA tetraloop has a quite different geometry, with the bases of T2, T3 and T4 stacking on each other, and with T4 pairing with T1 through a non-Watson-Crick base pair [4] (Figure 1B)
Summary
Tetraloop-receptor interactions are common and well-studied organizers of RNA tertiary structure. The UNCG tetraloop forms an especially stable structure [2,3], with its closing nucleotides T1 and T4 forming a U-G base pair, and T2 and T3 extending on either side of the backbone (Figure 1A). GNRAtype structures can be formed by longer loops (GNR[Xn]A), and nonadjacent nucleotides can come together to form GNRA-like tetraloop geometries (GN/RA, where ‘‘/’’ indicates a sequence break) [6]. Other less common tetraloop motifs have been identified and studied, including CUUG, ANYA and AUCG [1,7,8,9], but they do not typically form interactions with receptors
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