In the crystal structures of protein complexes with B-DNA, alpha and gamma DNA backbone torsion angles often exhibit non-canonical values. It is not known if these alternative backbone conformations are easily accessible in solution and can contribute to the specific recognition of DNA by proteins. We have analysed the coupled transition of the alpha and gamma torsion angles within the central GpC step of a B-DNA dodecamer by computer simulations. Five stable or metastable non-canonical alpha/gamma sub-states are found. The most favourable pathway from the canonical alpha/gamma structure to any unusual form involves a counter-rotation of alpha and gamma, via the trans conformation. However, the corresponding free energy indicates that spontaneous flipping of the torsions is improbable in free B-DNA. This is supported by an analysis of the available high resolution crystallographic structures showing that unusual alpha/gamma states are only encountered in B-DNA complexed to proteins. An analysis of the structural consequences of alpha/gamma transitions shows that the non-canonical backbone geometry influences essentially the roll and twist values and reduces the equilibrium dispersion of structural parameters. Our results support the hypothesis that unusual alpha/gamma backbones arise during protein-DNA complexation, assisting the fine structural adjustments between the two partners and playing a role in the overall complexation free energy.