Heat acclimation confers acquired thermotolerance (AT), and heat-acclimation memory (HAM) is the maintenance of AT for some time. In Arabidopsis and rice, the heat-stress-associated 32-kDa protein (HSA32) and heat shock protein101 (HSP101), a protein disaggregase, form a positive-feedback loop at the protein level to maintain AT; HSA32 mitigates HSP101 degradation, and HSP101 positively regulates the accumulation of HSA32. Here, we report the underpinning mechanism regarding how HSP101 affects the HSA32 level in Arabidopsis. We found that, without HSP101, nascent HSA32 was rapidly degraded, and the degradation was inhibited by the proteasome inhibitor, bortezomib, but independent of polyubiquitination. In response to heat stress, nascent HSA32 was present in liquid condensates and diffused in the cytosol after returning to non-stress temperature. Proximity labeling with TurboID fused to HSA32 identified HSP101 and five other protein chaperones and co-chaperones as the primary interactors. Notably, HSA32 interactors include three subunits of the cytosolic chaperonin involved in de novo protein folding. Disturbing the interaction between HSA32 and HSP101 destabilized HSA32 and compromised HAM. HSA32 is predicted as a TIM-barrel protein with three intrinsically disordered regions of high aggregation propensity. Recombinant HSA32 expressed in E. coli was partitioned into insoluble fractions. These observations suggest that HSA32 is aggregation-prone. Altogether, our findings highlight how plant stress memory is maintained by the mutual stabilization of two positive feedback components.