G-quadruplexes (G4) are four stranded nucleic acid structures formed by Guanine (G) rich sequences. DNA G4s are essential motifs in molecular biology performing a wide range of functions enabled by their unique and diverse structures. G4s are implicated in the genome instability, telomere maintenance, regulation of transcription, chaperoning activity, liquid-liquid phase separation and G4s are also considered as excellent drug targets. In genome, G4s coexist with double stranded duplex DNA. In this study, we focus on the conformational plasticity of the most abundant and biologically relevant parallel G-quadruplex topology. A multi pronged approach of structure survey, solution-state NMR spectroscopy and molecular dynamics simulations unravel subtle yet essential features of the parallel G-quadruplex topology. Stark differences inflexibility are observed for the nucleotides depending upon their positioning in the tetrad planes that are intricately correlated with conformational sampling of the propeller loop. Importantly, the terminal nucleotides in the 5’-end versus 3’-end of the parallel quadruplex display differential dynamics that manifests the ability to accommodate a duplex on either end of the G4. The conformational plasticity characterized in this study provides essential cues towards biomolecular processes such as small molecular binding, intermolecular G4 stacking and implications on how a duplex influences the structure of a neighboring quadruplex.