Phenotypic plasticity, in response to adverse conditions, determines plant productivity and survival. The aim of this study was to test if two highly productive Populus genotypes, characterised by different in vitro etiolation patterns, differ also in their responses to hormones gibberellin (GA) and abscisic acid (ABA), and to a GA biosynthesis inhibitor paclobutrazol (PBZ). The experiments on shoot cultures of ‘Hybrida 275′ (abbr. H275; Populus maximowiczii × P. trichocarpa) and IBL 91/78 (Populus tremula × P. alba) were conducted by either modulating the physical in vitro environment or by adding specific chemicals to the nutrient medium. Our results revealed two main sets of differences between the studied genotypes in environmental and hormonal regulation of growth responses. First, the genotype H275 responded to darkness with PBZ-inhibitable shoot elongation; in contrast, the elongation of IBL 91/78 shoots was not affected either by darkness or PBZ treatment. Secondly, the explants of H275 were unable to recover their growth if it was inhibited with ABA; in contrast, those of IBL 91/78 recovered so well after the temporal inhibition by ABA that, when rooted subsequently, they developed longer shoots and roots than without a previous ABA treatment. Our results indicate that GA catabolism and repressive signalling provide an important pathway to control growth and physiological adaptation in response to immediate or impending adverse conditions. These observations can help breeders define robust criteria for identifying genotypes with high resistance and productivity and highlight where genotypes exhibit susceptibility to stress.