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Author summary Plants must constantly regulate the allocation of resources between photomorphogenesis and defense signaling. Although light is known to influence plant defense, the underlying mechanisms remain largely unknown. Here we show that light plays specific and direct signaling roles in plant defense. Specifically, a positive role for COP1 E3 ligase, an important regulator of photomorphogenesis, in plant defense is demonstrated. We further show that COP1 regulates the levels of double-stranded RNA binding proteins DRB1 and DRB4, which in turn regulate the levels of resistance protein HRT that confers resistance against turnip crinkle virus. In contrast to COP1, a multi-subunit E3 ligase encoded by anaphase-promoting complex (APC) 10 negatively regulates DRB4 but had no effect on DRB1 levels. Together, these results suggest that COP1-mediated positive regulation of HRT is dependent on a balance between COP1 and negative regulators that target DRB1 and DRB4.