Signaling from Plastid Genome Stability Modulates Endoreplication and Cell Cycle during Plant Development

Plastid-nucleus genome coordination is crucial for plastid activity, but the mechanisms remain unclear. By treating Arabidopsis plants with the organellar genome-damaging agent ciprofloxacin, we found that plastid genome instability can alter endoreplication and the cell cycle. Similar results are observed in the plastid genome instability mutants of reca1why1why3. Cell division and embryo development are disturbed in the reca1why1why3 mutant. Notably, SMR5 and SMR7 genes, which encode cell-cycle kinase inhibitors, are upregulated in plastid genome instability plants, and the mutation of SMR7 can restore the endoreplication and growth phenotype of reca1why1why3 plants. Furthermore, we establish that the DNA damage response transcription factor SOG1 mediates the alteration of endoreplication and cell cycle triggered by plastid genome instability. Finally, we demonstrate that reactive oxygen species produced in plastids are important for plastid-nucleus genome coordination. Our findings uncover a molecular mechanism for the coordination of plastid and nuclear genomes during plant growth and development. [Display omitted] •Plastid genome instability alters endoreplication and cell cycle•Plastid genome instability results in increased expression of cell-cycle-related genes•SOG1 mediates the activation of cell-cycle-related genes by plastid genome instability•ROS is required for communication of plastid genome with endoreplication and cell cycle Duan et al. show that plastid genome instability modulates endoreplication and cell-cycle progression by plastid-to-nucleus retrograde signaling through the SOG1-mediated pathway, which is required for plant growth and development.