It is shown that the phosphate-methylated DNA miniduplex d(CpG)2 adopts a left-handed Z-type structure, whereas the phosphate-methylated miniduplex d(GpC)2 is right-handed. Furthermore, it is shown that elongation of the systems to the tetramer level results in right-handed duplexes with rather low stability. The phosphate-methylated hexamer d(CpGpCpGpCpG) is present in the single-strand form. It is suggested that these results are of interest in the understanding of the exact role of salt cations in stabilizing the Z-DNA structure of natural duplexes d(CpG…CpG)2 in high salt solution, since the methylated phosphate groups in fact mimic the situation of complete phosphate-charge shielding. Therefore, it is concluded that exclusive cation-phosphate complexation in the d(CpG)2 segments stabilizes the Z structure. 31P-NMR experiments on the natural duplex d(CpGpCpGpCpG)2 at different concentrations of Mg2+ provided independent proof for the proposed model.