Prolongation of the light period causes photoperiod stress in plants. The response to photoperiod stress includes the induction of a distinct set of stress marker genes, of reactive oxygen species (ROS), and of stress hormones. In this study, the impact of light intensity and light quality on the photoperiod stress response was investigated. A threshold light intensity of circa 50 μmol m−2 s−1 is necessary for inducing photoperiod stress, indicating the involvement of chloroplasts. Lower photoperiod stress symptoms in retrograde signaling mutants (gun4, gun5) and mutants with constrained plastid function (glk1 glk2) corroborated the role of chloroplasts. Genetic analysis revealed that the photoreceptors phyB and particularly CRY2 are important to perceive photoperiod stress. Overall, these results showed that both plastid-dependent and photoreceptor-dependent signaling pathways are involved in sensing the light conditions causing photoperiod stress and governing the response to it.