Chloroplast state transitions modulate nuclear genome stability via cytokinin signaling in Arabidopsis

Activities of the chloroplasts and nucleus are coordinated by retrograde signaling, which play crucial roles in plant development and environmental adaptation. However, the connection between chloroplast status and nuclear genome stability is poorly understood. Chloroplast state transitions enable the plant to balance photosystem absorption capacity in an environment with changing light quality. Here, we report that abnormal chloroplast state transitions lead to instability in the nuclear genome and impaired plant growth. We observed increased DNA damage in the state transition-defective Arabidopsis thaliana mutant stn7, and demonstrated that this damage was triggered by cytokinin accumulation and activation of cytokinin signaling. We showed that cytokinin signaling promotes a competitive association between ARABIDOPSIS RESPONSE REGULATOR 10 (ARR10) with PROLIFERATING CELLULAR NUCLEAR ANTIGEN 1/2 (PCNA1/2), inhibiting the binding of PCNA1/2 to nuclear DNA. This affects DNA replication, leading to replication-dependent genome instability. Treatment with 2,5-dibromo-3-methyl-6-isopropylbenzoquinone that simulates the reduction of the plastoquinone pool during abnormal state transitions increased the accumulation of ARABIDOPSIS HISTIDINE-CONTAINING PHOSPHOTRANSMITTER 1, a phosphotransfer protein involved in cytokinin signaling, and promoted the interaction between ARR10 with PCNA1/2, leading to increased DNA damage. These findings highlight the function of cytokinin signaling in coordinating chloroplast function and nuclear genome integrity during plant acclimation to environmental changes.