Recent work with intrinsically disordered proteins (IDPs) has projected a myriad of their survival instincts based mainly on the total charge content, the abundance of polar residues, and the paucity of hydrophobic amino acids. This work uses a plant IDP AtPP16-1 (Arabidopsis thaliana phloem protein class 16-1), whose solution NMR structure was determined by us recently, to show legitimate negative thermal expansion (NTE) of the native state. The thermal expansion continues to be negative even as the tertiary structure is perturbed by ultralow levels of urea up to 0.4 M. The NTE of these subdenatured states is called apparent NTE because they are prone to undergo conformational changes with temperature. Hydrodynamic shrinkage of the NTE IDP is also observed by dynamic light scattering (DLS) and NMR-measured global rotational correlation time (τc). The protein with denatured tertiary structure but otherwise preserved native-state secondary structure collapses to a dynamically rigid state. The data are mainly based on thermal coefficients of chemical shift and nuclear relaxation measured by heteronuclear NMR. The hydrodynamic shrinkage and collapse under marginally varying solvent compositions that may arise from unstable tertiary structure and dynamic disorder of chain segments across the backbone could be a generic property of IDPs.