When exposed to shade from neighbours, competitive plants modify their growth patterns to improve access to light. In dense plant stands, ranging from forests to humid grasslands and crops, shade is interrupted by sunflecks penetrating the canopy. Relatively infrequent, minute-scale interruptions can significantly contribute to the daily light input. However, given the short duration and the time gap between these low frequency sunflecks (LFS), whether plants can sense them was unknown. Here, we demonstrate that phytochrome B (phyB), cryptochrome 1 (cry1), cry2 and UV RESISTANCE LOCUS 8 (UVR8) cooperatively perceive LFS to reduce hypocotyl growth in Arabidopsis thaliana. LFS also enhanced the expression of photosynthetic and photo-protective genes and initiated pre-emptive acclimation to water restriction. Repeated LFS increased the nuclear abundance of cry1 and UVR8. This positive feedback enhanced the sensitivity to subsequent LFS and even to the shade between LFS. LFS reduced the nuclear abundance of the growth regulator PHYTOCHROME INTERACTING FACTOR 4 (PIF4), which only slowly recovered upon return to shade, further amplifying the signal. Our findings unveil hitherto uncharacterised dynamics of cry1, UVR8 and PIF4 under fluctuating light. This photosensory system helps adjust plants to the prevailing environmental conditions.