The heterotrimeric guanine nucleotide-binding protein (G-protein) has been demonstrated to mediate various signaling pathways in plants. However, its role in phytochrome A (phyA) signaling remains elusive. In this study, we discover a new phyA-mediated phenotype designated far-red irradiation (FR) preconditioned cell death, which occurs only in the hypocotyls of FR-grown seedlings following exposure to white light (WL). The cell death is mitigated in the G alpha mutant gpa1 but aggravated in the G beta mutant agb1 in comparison with the wild type (WT), indicative of antagonistic roles of GPA1 and AGB1 in the phyA-mediated cell-death pathway. Further investigation indicates that FR-induced accumulation of nonphotoconvertible protochlorophyllide (Pchlide633), which generates reactive oxygen species (ROS) on exposure to WL, is required for FR-preconditioned cell death. Moreover, ROS is mainly detected in chloroplasts using the fluorescent probe. Interestingly, the application of H2O2 to dark-grown seedlings results in a phenotype similar to FR-preconditioned cell death. This reveals that ROS is a critical mediator for the cell death. In addition, we observe that agb1 is more sensitive to H2O2 than WT seedlings, indicating that the G-protein may also modify the sensitivity of the seedlings to ROS stress. Taking these results together, we infer that the G-protein may be involved in the phyA signaling pathway to regulate FR-preconditioned cell death of Arabidopsis hypocotyls. A possible mechanism underlying the involvement of the G-protein in phyA signaling is discussed in this study.