The COP9 (constitutive photomorphogenesis 9) signalosome (CSN) is an evolutionary conserved protein complex which regulates various growth and developmental processes. We used CSN hypomorphic mutants to study the role of CSN in plant responses to environmental stress, and found that heat stress specifically enhances the growth of csn5a-1, but not growth of other hypomorphic mutants (csn1-10 and csn5b-1) or photomorphogenesis repressor mutants (cop1-4 and spa triple mutant (spa1 spa3 spa4)). Following heat stress, csn5a-1 exhibit an increase in cell size, ploidy, photosynthetic activity, number of lateral roots, and an up-regulation of genes connected to cell cycle progression and auxin response. Studies using DR5::N7 VENUS and DII-VENUS reporter constructs indicate that the heat-induced growth is likely due to an increase in auxin signaling. The heat stress leads to a degradation of the DII-VENUS signal, and this signal recovers in 3D after heat treatment in the WT, but not in csn5a-1. This suggests a role of CSN5A in AUX/IAA recovery to regulate auxin homeostasis in Arabidopsis