The proper regulation of cell-cycle regulators is curial for both viral replication and host-plant adaptive growth during the viral pathogenesis. Mechanisms on reorchestrating RETINOBLASTOMA-RELATED 1 (RBR1), repressor of E2F transcription factor, and downstream genes in host-virus interactions are unclear. Here, we discover that anaphase-promoting complex/cyclosome (APC/C) E3 ligase activator cell division cycle 20 (CDC20) in tomato binds RBR1 or mediates cyclin D1 depletion to preserve RBR1-E2F complexes, while geminivirus or crinivirus repurposes APC/C activities to liberate E2Fs in two ways: activating APC/C to deplete RBR1 or blocking APC/C to stimulate cyclin-D1-mediated RBR1 depletion. The liberated E2Fs activate DNA polymerase or heat shock protein 70 gene transcription to favor virus propagation. The improper disruption of RBR1-E2F complexes via hijacking APC/C causes the host growth repression. We uncover a scenario in which the virus co-opts host APC/C to reprogram RBR1-E2F complex to favor its propagation while dampening host vitality.
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