Chloroplast State Transitions Modulate Nuclear Genome Stability via Cytokinin Signaling in Arabidopsis

Activities of the chloroplasts and nucleus are coordinated by retrograde signaling, which has crucial roles in plant development and environmental adaptation. However, the connection between chloroplast status and nuclear genome stability is not well understood. Chloroplast state transitions allow the plant to balance the absorption capacity of the photosystems in an environment in which the light quality was changing. Here we demonstrate that abnormal chloroplast state transitions lead to instability of the nuclear genome and impaired plant growth. We observed increased DNA damage in the state transition-defective Arabidopsis (Arabidopsis thaliana) mutant stn7; this damage was triggered by cytokinin accumulation and activation of cytokinin signaling. We propose that cytokinin signaling promotes the competitive association of ARABIDOPSIS RESPONSE REGULATOR 10 (ARR10) with PROLIFERATING CELLULAR NUCLEAR ANTIGEN 1/2 (PCNA1/2), thereby 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, which 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 of ARR10 with PCNA1/2, leading to DNA damage. These findings highlight the role of cytokinin signaling in coordinating chloroplast function and nuclear genome integrity during plant acclimation to environmental changes.