Properties of the Nucleic-acid Bases in Free and Watson-CrickHydrogen-bonded States: Computational Insights into theSequence-dependent Features of Double-helical DNA

A. R. Srinivasan1, Ronald R. Sauers1, Marcia O. Fenley3,4, Alexander H. Boschitsch5,Atsushi Matsumoto1,6,7, Andrew V. Colasanti1,‡, and Wilma K. Olson1,2,*1 Department of Chemistry & Chemical Biology, Rutgers, the State University of New Jersey,Wright-Rieman Laboratories, 610 Taylor Road, Piscataway, NJ 08854-8087, USA2 BioMaPS Institute for Quantitative Biology, Rutgers, the State University of New Jersey, Wright-Rieman Laboratories, 610 Taylor Road, Piscataway, NJ 08854-8087, USA3 Department of Physics, Florida State University, Tallahassee, FL 32306-4380, USA4 Institute of Molecular Biophysics, Florida State University, Tallahassee, FL 32306-4380, USA5 Continuum Dynamics, Inc. 34 Lexington Avenue, Ewing, NJ 08618-2302, USA6 Quantum Bioinformatics Team, Center for Computational Science and Engineering, QuantumBeam Science Directorate, Japan Atomic Energy Agency, 8-1 Umemidai, Kizugawa, Kyoto,619-0215, Japan7 Research Unit for Quantum Beam Life Science Initiative, Quantum Beam Science Directorate,Japan Atomic Energy Agency, 8-1 Umemidai, Kizugawa, Kyoto, 619-0215, Japan

AbstractThe nucleic-acid bases carry structural and energetic signatures that contribute to the uniquefeatures of genetic sequences. Here we review the connection between the chemical structure ofthe constituent nucleotides and the polymeric properties of DNA. The sequence-dependentaccumulation of charge on the major- and minor-groove edges of the Watson-Crick base pairs,obtained from ab initio calculations, presents unique motifs for direct sequence recognition. Theoptimization of base interactions generates a propellering of base-pair planes of the samehandedness as that found in high-resolution double-helical structures. The optimized base pairsalso deform along conformational pathways, i.e., normal modes, of the same type induced by thebinding of proteins. Empirical energy computations that incorporate the properties of the basepairs account satisfactorily for general features of the next level of double-helical structure, butmiss key sequence-dependent differences in dimeric structure and deformability. The latterdiscrepancies appear to reflect factors other than intrinsic base-pair structure.

Keywordsab initio calculations; DNA base pairs; conformation; electronic structures; electrostatic potentialsurfaces; normal modes

*To whom correspondence should be addressed: Tel: 732-445-3993; Fax: 732-445-5958; wilma.olson@rutgers.edu.‡Current address: Provid Pharmaceuticals Inc., 671 U.S. Route 1, North Brunswick, NJ 08902.

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Published in final edited form as:Biophys Rev. 2009 March 1; 1(1): 13–20. doi:10.1007/s12551-008-0003-2.

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IntroductionThe energetic and structural information encoded in the DNA base-pair sequence has directbearing on the overall shape and stability of the double-helical molecule. The basis of thiscode lies in the electronic characteristics of the heterocyclic bases — adenine (A), thymine(T), guanine (G), and cytosine (C) —and their hydrogen-bonded Watson-Crick complexes(Figure 1). Although much of the net negative charge per nucleotide is concentrated on thephosphate group, there is a build-up of appreciable fractional charge on certain atoms of theheterocyclic bases. This article highlights a number of factors — partial atomic charges,intrinsic structures, binding energies, dipole moments, electrostatic potential surfaces, andrigid-body motions — that distinguish the two Watson-Crick base pairs and drawsconnections between these local chemical features and the higher-order structuralinformation that is used to recognize and process the genetic information stored in longbase-pair sequences. The capability to link basic chemical information with the polymericproperties of DNA rests upon technical advances that make it possible (i) to determine, withhigh accuracy, the electronic structures of hydrogen-bonded base complexes (Frisch et al.2001;Frisch et al. 2003), (ii) to represent the electrostatic potential of the base pairs at highresolution (Boschitsch et al. 2002;Boschitsch and Fenley 2004), and (iii) to compare thesechemical features with relevant spatial information (Lu and Olson 2003;Lu and Olson 2008)in the growing database of high-resolution nucleic-acid structures (Berman et al. 1992) andwith classic physical measurements.

Atomic charge distributionImportantly, the distributions of electronic charge on the Watson-Crick base pairs differfrom those on the free bases (see the Supplementary Materials for a complete list of theatomic charges of base and base-pair atoms obtained within the Gaussian 98 and Gaussian03 suites of programs (Frisch et al. 2001; Frisch et al. 2003)). The characteristicaccumulation of electronic charge on the exposed major- and minor-groove edges of thebase pairs presents unique motifs for direct sequence recognition (Seeman et al. 1976). Forexample, the much larger negative charge on the C5 atom of cytosine compared to thecorresponding atom of thymine, e.g., −0.69 vs. −0.22 esu in the Watson-Crick pairs,influences the interactions of charged ligands with the major-groove edges of the twopyrimidines (see below).

These and other subtleties in local electronic structure surface at the base-pair level in termsof distinctly different A·T and G·C dipoles, with the computed magnitude of the G·C dipolemore than double that of the A·T pair (6.6. vs. 2.4 Debye). Confidence in these predictions isstrengthened by the agreement between the computed dipole moment of free adenine (3.0Debye) and the measured dipole moment (3.0±0.2 Debye) of 9-n-butyl-adenine in CCl4(DeVoe and Tinoco Jr. 1962). On the other hand, the predicted dipole moment of guanine(7.2 Debye) exceeds the reported value (5.5 Debye) (Párkányi et al. 2002). The lattermeasurement, performed in dioxane, is not directly relevant to the computations in that thepolar solvent may form hydrogen bonds with the base and thereby perturb its electronicstructure. No such interactions occur in the non-polar CCl4 solvent. The orientations anddirections of the computed dipole moments, depicted in Figures 2 and 3 by black arrows,point to the unique electronic character of the free bases as well as the base pairs.

Base-pair non-planarityConventional wisdom attributes the (negative) propeller twisting of the Watson-Crick basepairs seen in high-resolution DNA structures to a base-stacking effect, i.e., the out-of-planerotation of complementary bases about the long base-pair axis seemingly enhances stackingoverlaps with bases in adjacent residues (Levitt 1978); see illustrative image of propeller-

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twisted base-pair planes in Figure 4. Calculations, however, show that negative propellertwist is intrinsic to isolated, unstacked A·T and G·C pairs and is a direct consequence of thepyramidal geometry of the proton-donating, exocyclic amino groups — an idea anticipatedin earlier research (Komarov and Polozov 1990).

The displacement of the amino hydrogens out of the starting plane introduces non-zerovalues of propeller twist while concomitantly lowering the binding energy. For example, theA·T pair takes on negative propeller values and the energy drops by −1.2 kcal/mole if thehydrogens attached to N6 of adenine fall below the starting base-pair plane. The hydrogensattached to a negatively propellered G·C pair, by contrast, lie above the starting plane owingto the different placement of the amino group on the G·C pair. The energy decrease in thepropeller-twisted G·C pair, −1.0 kcal/mole, is not quite as pronounced as that of thesimilarly deformed A·T pair.

The degree of nonplanarity in the derived base pairs, reported in Table 1 in terms of theexocyclic torsion angles described by relevant heavy atoms, agrees fairly well with the meanvalues found in ultra-high resolution structures of double-helical B-DNA, although the signsof rotation in the lowest-energy base-paired structures differ from the X-ray observations.The computed out-of-plane displacement of the exocyclic nitrogens in free, unpaired basestypically exceeds that in the paired bases, but there are no crystal data to test this prediction.The predicted displacement of nitrogen, however, is intermediate between that detected inneutron-diffraction studies of related compounds (McMullan et al. 1980;Weber et al.1980;Klooster et al. 1991) and that deduced from measurements of the direction of theinfrared transition moments of adenine and cytosine (Dong and Miller 2002;Choi et al.2005) (see Supplementary Materials for numerical values).

The predicted propeller twisting of the Watson-Crick base pairs, however, is lesspronounced than that found in well-resolved X-ray structures, particularly for A·T pairs(Table 1). In addition to the standard rationalization of DNA melting properties in terms ofthe number of hydrogen bonds in A·T vs. G·C base pairs, the calculations suggest that theremay be a built-in, sequence-dependent pressure for AT-rich DNA to disassemble moreeasily than GC-rich DNA. That is, the intrinsic structure of the free A·T base pair appears tobe more significantly compromised than that of the free G·C pair in duplex DNA. On theother hand, the conformational stiffness of so-called DNA A-tracts, i.e., short stretches of 4–6 consecutive A·T base pairs, is often attributed to the bifurcated hydrogen bonding madepossible by stacks of highly propeller-twisted A·T pairs (Nelson et al. 1987;Chan et al.1993). Such hydrogen-bond stabilization occurs as well in overtwisted CA·TG dimer steps(Timsit 1999), which are known to be highly deformable (Olson et al. 1998).

Sequence-dependent structure and deformationThe energy-optimized Watson-Crick base pairs show many of the same subtle, sequence-dependent conformational features found in high-resolution DNA structures (Table 1). Forexample, the G·C pair opens in the opposite sense from the A·T pair, concomitantlyshortening, straightening, and presumably strengthening the G(O6)···C(H41)–C(N4)interaction compared to the A(N6)–A(H61)···T(O4) hydrogen bond formed at thecorresponding major-groove location on A·T. The former interaction also appears to bestronger, in terms of its more nearly ideal geometry, than the G(N2)–G(H21)···C(O2)hydrogen bond located on the minor-groove side of the G·C pair. The stronger hydrogenbond contributes, in turn, to the strong G·C dipole noted above.

The predicted base-pair structures account as well for gas-phase measurements. Forexample, the angle between the planes of paired adenine and thymine, which can beextracted from the buckle and propeller angles, is remarkably similar to the dihedral angle

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estimated from the measured moments of inertia of 2-aminopyridine·2-pyridone, an analogof the A·T base pair, in the gas phase, i.e., 6.7° predicted vs. 6.1° found experimentally(Roscioli and Pratt 2003). The predicted length of the A(N1)···T(H3)–T(N3) hydrogen bondalso closely matches the value found in the same experiment, i.e., 2.87 Å computed vs.2.898 Å observed. The measured value of the A(N6)–A(H6)···T(O4) interaction, however, isless than that determined here, i.e., 2.81 Å observed vs. 2.99 Å computed (Roscioli and Pratt2003).

The global motions of the base pairs, deduced from the low-frequency normal modes of theenergy-minimized structures, also mimic the pattern of rigid-body variation observed inwell-resolved structures (see Supplementary Materials). That is, the buckling and propeller-twisting motions, seen to dominate the deformations of Watson-Crick base pairs in high-resolution protein-DNA structures, are of lower frequency (energy) than all other normalmodes. The predicted movements of base pairs are described in Figure 4 by a color-codedspectrum of normal modes dominated by fluctuations of one of the six complementary base-pair parameters. The least costly (lowest-frequency) modes are softer than the torsionalmodes of the C1′ methyl groups (with frequencies of ~50 cm−1). The stiffest rigid-bodymodes are comparable in frequency to the out-of-plane bending modes of individual bases(data not shown).

The buckling and propeller-twisting motions do not appreciably distort the hydrogenbonding of complementary bases and are relatively insensitive to base-pair composition. Bycontrast, the rigid-body deformations via more costly modes (opening, shear, or stretch),which have a greater effect on hydrogen-bond geometry, differ in A·T vs. G·C pairs. TheA·T pair deforms via stretch or opening much more easily than the G·C pair in both solid-state examples and the computed model, presumably reflecting the cost of distorting threeG·C vs. two A·T hydrogen bonds. Changes in shear are easier, however, for G·C than A·T,possibly taking advantage of shared/bifurcated hydrogen-bonding that is possible in G·C butnot A·T.

Electrostatic potential and base recognitionImages generated by color-coding biomolecular surfaces according to the electrostaticpotential have become extremely valuable in obtaining qualitative information aboutpreferred ligand (metal, drug, protein) binding sites and the degree of electrostaticcomplementarity between molecules involved in recognition and association processes(Honig and Nicholls 1995). Such is the case here for the isolated DNA bases and theWatson-Crick base pairs, which although electronically neutral, have distinct, sequence-dependent electrostatic fingerprints (Figures 2, 3). The distribution of hydrogen-bondingdonor and acceptor atoms on the edges of the heterocyclic species gives rise to well-definedpatterns of positive and negative electrostatic potential and confirm many of the generaltrends suggested by the very first calculations of the electrostatic potential from approximateatomic charges (Pullman et al. 1979; Lavery and Pullman 1981; Weiner et al. 1982).

The absolute potentials of selected donor and acceptor atoms on the isolated bases and basepairs immersed in a simulated aqueous medium (see Supplementary Materials) are fairlysmall because of the null net charges on these chemical species. Literature values of theelectrostatic potentials (Pullman and Pullman 1981; Weiner et al. 1982; Fogolari et al. 2002;Hud and Plavec 2003), based on various distributions of molecular charge, are typicallycomputed with a single low dielectric constant and thus of much greater magnitude.Published potential surfaces, based on two-dielectric Poisson-Boltzmann modeling of theDNA duplex and surrounding aqueous solvent, are of greater magnitude but of lower

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resolution than the current images. The earlier, more approximate surfaces, however, do notlend themselves to the quantitative descriptions of atomic surface potentials reported here.

The images and numerical data clearly show that (i) the minor-groove edge of the A·T pairis more electronegative than the major-groove edge, (ii) the major-groove side of guanine ismore electronegative than the minor-groove side, and (iii) the major-groove edge of cytosineis highly electropositive. The negative electrostatic potential of the A·T minor groovepresumably underlies the preferential binding of ions (Hud and Polak 2001) and smallcationic molecules, such as netropsin and distamycin (Kopka et al. 1985), and the specificityof cationic amino-acid side groups, such as those in the bacteriophage 434 repressor protein(Mauro and Koudelka 2004), for such sites. The deeper major-groove potential of the G·Cpair seemingly accounts for the well-known binding of small cations with the N7 and O6atoms on the major-groove edge of guanine (McFail-Isom et al. 1999; Auffinger andWesthof 2000; Hud and Polak 2001; Egli 2002; Subirana and Soler-López 2003). Thepositive potential on cytosine forms the basis for the many close contacts of small inorganicanions with the C(N4) atom in nucleic-acid structures (Auffinger et al. 2004) and thefrequent participation of the C(C5) atom in ‘weak’ C–H···O hydrogen bonds with boundproteins (Mandel-Gutfreund et al. 1998). The anionic amino acids, aspartic acid andglutamic acid, have long been expected to bind to the amino groups on A and C (Suzuki1994).

The conventional assignment of the same sets of partial charges to free and paired nucleic-acid bases ignores the neutralization of the electrostatic potential surface upon base-pairformation. The strength of the potentials on the Watson-Crick edges of the free basesostensibly contributes to both base-pair formation and ligand-binding specificity. Forexample, the highly electronegative N3 of the unpaired, catalytically-essential cytosine 75 ofthe hepatitis delta virus ribozyme acts as a general base, accepting a proton from thesubstrate 2′-OH during phosphate cleavage (Ke et al. 2004), and the exposed electropositiveN1 (NH) and N2 (NH2) atoms of unpaired guanines often donate hydrogens to the anionicside-chain carboxyl of glutamic acid in protein-RNA structures (Kim et al. 2003), includingthe trp RNA-binding attenuation protein (Antson et al. 1999) and various tRNA synthetases(Yaremchuk et al. 2001), and in the structures of proteins complexed with small guanine-containing ligands (Nobeli et al. 2001).

Binding energiesIn addition to reproducing high-resolution structural data, the calculations reviewed hereaccount satisfactorily for many of the traditional physical benchmarks used to assesscomputational reliability. For example, the Watson-Crick binding energies match gas-phaseobservations, −13.0 kcal/mole for A·T and −21.0 kcal/mole for G·C (Yanson et al. 1979).The calculated values, −14.3 kcal/mole for A·T and −25.0 kcal/mole for G·C, however,exceed the recent findings of Jurecka and Hobza (−15.4 and −28.3 kcal/mole, respectively)(Jurecka and Hobza 2003), who assert that their results represent the lower boundaries of thetrue stabilization energies.

Electronic structure and large-scale computationThe future promise of atomic-level simulations in deciphering the sequence-dependentproperties of DNA rests on continuing improvements of the force fields that underlie thecalculations. The configurations and charges of the Watson-Crick base pairs presented hereaccount for general features in the next level of double-helical structure, i.e., the preferredarrangements of neighboring base pairs, but miss key sequence-dependent differences inintrinsic structure and deformability. Correct predictions include (i) the anisotropy of DNAbending, i.e., preferable deformation via roll as opposed to tilt, (ii) the relative ease of

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bending compared to twisting, and (iii) the preferential displacement of base pairs via shiftand slide. The predicted sense of AA·TT vs. GG·CC deformation, however, is incorrect (seeSupplementary Materials).

The A·T base pair adopts a different, more highly propellered arrangement within double-helical structures that appears to contribute to the observed stiffness of AA·TT compared toGG·CC dimers. High-resolution DNA structures also reveal a sequence-dependent build-upof water molecules and amino acid residues around the nucleic-acid bases (unpublisheddata). Approximation of these features through reduction of the base-pair chargescontributes to the ‘A-philicity’ of GG·CC compared to AA·TT steps (Ivanov andMinchenkova 1995), i.e., the tendency of the GG·CC dimer to assume positive roll anglesthat close the major groove and negative values of slide that displace the G·C pairs withrespect to the double-helical axis and concomitantly deepen the major groove. Interestingly,previous calculations that successfully mimicked the tendencies of GG·CC dimers to adoptA-like conformational states, treated the partial charges of base atoms with a less polar,albeit highly approximate Poltev charge set (Zhurkin et al. 1980) and approximated theintervening solvent with a sigmoidal, distance-dependent dielectric constant (Mazur et al.1989). The appropriate balance of charge on the DNA bases, backbone, and surroundingchemical environment is key to the correct prediction of DNA fine structure andinteractions.

Supplementary MaterialRefer to Web version on PubMed Central for supplementary material.

AcknowledgmentsThe U.S. Public Health Service (research grant GM20861 to WKO) and the National Science Foundation (AdvanceFellows Award 0137961 to MOF) have generously supported this work. We thank Dr. Suse Broyde for helpfuldiscussions and Mr. Mauricio Esguerra for the scripts used to extract files from structural databases.

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Figure 1.Comparative hydrogen-bonding interactions, chemical structures (including double bonds),and displacement of bases comprising normal A·T and G·C Watson-Crick pairs. Hydrogenbonds are designated by dashed lines and the ‘weak’ CH···O bond of the A·T base-pair by athin wavy line. Conventional proton donor and acceptor atoms are colored red and blue,respectively. The donor and acceptor atoms involved in ‘weak’ CH···O interactions aresimilarly highlighted in magenta and cyan. The line joining C1′ atoms on associated basesillustrates the isomorphous geometry of the Watson- Crick pairs, with roughly equivalentangles λB (B = A, T, G, C) formed between the long, finely dotted C1′···C1′ virtual bond andeach of the C1′–N9 and C1′–N1 glycosidic bonds. Atoms with partial charge differences of±0.05 esu or more in the base-paired vs. base-separated state are highlighted by gray shading

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Figure 2.Electrostatic potential surfaces of the methylated (purine N9 and pyrimidine N1) form of anoptimized A·T base pair and its adenine (left) and thymine (right) components in a simulatedaqueous environment. Views looking down the major- and minor-groove edges (top andbottom rows of images, respectively) and perpendicular to the base and base-pair planes(middle row). White wireframe models of the respective molecules are superimposed on theelectrostatic potential surfaces. Dipole-moment vectors, noted by black arrows, are drawn inaccordance with the computed structure and charges. The surfaces of bases and base pairsare color-coded such that the areas of greatest negative potential (–1 kcal/mole) are yellow,those of greatest positive potential (+1 kcal/mole) are green, and the intermediate regions ofnegative, neutral, and positive potential vary respectively from red to white and blue. SeeSupplementary Materials for further details.

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Figure 3.Electrostatic potential surfaces of the methylated (purine N9 and pyrimidine N1) form of anoptimized G·C base pair and its guanine (left) and cytosine (right) components. See legendto Figure 2.

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Figure 4.Color-coded spectrum of the lowest frequency normal modes of A·T and G·C hydrogen-bonded Watson-Crick base pairs. The color coding denotes the base-pair fluctuations thatdominate the respective modes: buckle (orange): propeller (yellow); opening (green); shear(deep blue); stretch (magenta); stagger (light blue). The normal modes, expressed in theGaussian package (Frisch et al. 2001; Frisch et al. 2003) in terms of individual atomicdisplacements, are translated to fluctuations of base-pair parameters with the 3DNAsoftware (Lu and Olson 2003). Structural distortions are modeled by moving the atomsalong the predicted displacement vectors for each normal mode, such that the energies of thedistorted structures are increased by kBT/2 over that of the minimum-energy structure, wherekB is the Boltzmann constant and T the absolute temperature. The differences between thebasepair parameters of the distorted structures and the minimum-energy structure providethe basis for the described motions. A pictorial definition of each base-pair parameter(illustrating positive values) is shown at the top.

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Table 1

Comparative geometric features of complementary Watson-Crick base pairs in energy-optimized and high-resolution B-DNA crystal structures.1

A·T G·C

Computation X-ray Computation X-ray

Base-pair parameters2

Buckle −5.7 +1.5(±5.6) +7.0 +4.6 (±6.6)

Propeller −3.6 −13.8 (±5.4) −7.3 − 8.7 (±5.9)

Opening +0.3 +2.3 (±4.2) −1.7 −0.1 (±3.0)

Shear +0.03 +0.06 (±0.31) −0.20 −0.18 (±0.20)

Stretch −0.08 −0.12 (±0.14) −0.08 −0.14 (±0.14)

Stagger +0.10 +0.06 (±0.21) +0.04 +0.15 (±0.25)

Virtual inter-base parameters3

dC1′··· C1′ 10.54 10.47 (±0.22) 10.72 10.62 (±0.17)

λY 56.1 55.5 (±3.4) 55.2 55.2 (±2.2)

λR 55.7 55.9 (±2.7) 54.0 54.8 (±2.7)

Hydrogen-bond lengths

C2–H···O2 3.60 3.54 (±0.21) – –

N1···H–N3 2.87 2.83 (±0.13) – –

N6–H···O4 2.99 3.04 (±0.17) – –

N2–H···O2 – – 2.96 2.81 (±0.14)

N1–H···N3 – – 2.97 2.90 (±0.11)

O6···H–N4 – – 2.85 2.92 (±0.16)

Exocyclic torsions4

Adenine

C4–C5–C6–N6 −178.1 (+178.0) 177.3 (±2.2) – –

C2–N1–C6–N6 +178.1 (−178.1) – –

−178.1 (±1.3)

Guanine

C6–N1–C2–N2 – – +176.2 (−176.3) −179.9 (±1.6)

C4–N3–C2–N2 – – −175.9 (+176.0) 178.6 (±2.2)

Cytosine

C2–N3–C4–N4 – – −179.8 (+179.8) −178.9 (±2.5)

C6–C5–C4–N4 – – −179.7 (+179.7) 178.9 (±2.3)

1Predicted structures obtained from calculations based on second-order Møller-Plesset perturbation theory within the Gaussian 98 and Gaussian 03

suites of programs (Frisch et al. 2001; Frisch et al. 2003). Except where noted, X-ray data based on the analysis, within 3DNA (Lu and Olson2003), of (181 A·T and 168 G·C) Watson-Crick base pairs in 78 B-DNA crystal structures of 2.0 Å or better resolution without chemicalmodification, mismatches, drugs, or proteins from the Nucleic Acid Database (Berman et al. 1992). ‘Weak’ C–H···O distances taken from 181 A·Tpairs in 58 structures. Mean values and standard deviations (subscripted values in parentheses) exclude chemically modified bases, terminal andpenultimate base pairs, side groups attached to nicked backbone strands, and base pairs that stacked against modified or mispaired 3′- and 5′-nucleotides. All angles expressed in degrees and distances in Ångstrom units.

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2See schematic illustrations in Figure 4 for parameter definitions. Values given here for purine·pyrimidine (A·T and G·C) pairs are identical to

those of the corresponding pyrimidine·purine (T·A and C·G) pairs, except that buckle and shear are of the opposite sign.

3Virtual angles λY = ∠N1(Y)–C1′(Y)···C1′(R) and λR = ∠N9(R)–C1′(R)···C1′(Y) describe the pivoting of complementary bases in the base-pair

plane (Figure 1). Virtual distance dC1′··· C1′ measures base-pair width.

4Predicted torsions in parentheses correspond to base pairs in a secondary, higher energy minimum with positive propeller twist. Observations

come from analyses of the specified paired base in ultra-high resolution (0.99 Å or better resolution) B-DNA crystal structures: 27 A·T pairs from16 structures and 36 G·C pairs from 15 structures. described motions. A pictorial definition of each base-pair parameter (illustrating positivevalues) is shown at the top.

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