Environmental challenges such as low light intensity induce differential growth-driven upward leaf movement (hyponastic growth) in Arabidopsis thaliana. However, little is known about the physiological regulation of this response. Here, we studied how low light intensity is perceived and translated into a differential growth response in Arabidopsis. We used mutants defective in light, ethylene and auxin signaling, and in polar auxin transport, as well as chemical inhibitors, to analyze the mechanisms of low light intensity-induced differential growth. Our data indicate that photosynthesis-derived signals and blue light wavelengths affect petiole movements and that rapid induction of hyponasty by low light intensity involves functional cryptochromes 1 and 2, phytochrome-A and phytochrome-B photoreceptor proteins. The response is independent of ethylene signaling. Auxin and polar auxin transport, by contrast, play a role in low light intensity-induced differential petiole growth. We conclude that low light intensity-induced differential petiole growth requires blue light, auxin signaling and polar auxin transport and is, at least in part, genetically separate from well-characterized ethylene-induced differential growth.