Photosynthesis and translation are targets of metabolic control and development in plants. Here, we described an antiviral immunity circuit, NIK1/RPL10/LYMYB, which ties the photosynthetic function to translational control in response to biotic and abiotic signals. We first examined the viral PAMPs that activate the antiviral signaling module by mediating coreceptor NIK1 phosphorylation and subsequent activation of the associated readouts. Then, we used CRISPR-Cas to target receptor-like kinases and define viral PAMP recognition receptors. Furthermore, we showed that the downstream component of the NIK1/RPL10 antiviral signaling module, LIMYB, which represses translational machinery-related gene expression and translation, also suppresses photosynthetic apparatus-related genes leading to inhibition of the photosynthetic function. The activity of LIMYB, which was regulated by phosphorylation, was the primary determinant for the decrease in electron transport rate, exchange gas parameters, quantum efficiency, and water-use efficiency in the LIMYB-overexpressing lines. The decreased photosynthetic activity was linked to the NIK1 antiviral signaling and stunted growth. NIK1 activation by viral PAMPs, or expressing a constitutively activated NIK1 mutant, T474D, repressed the photosynthesis-related marker genes and inhibited the photosynthetic function in control lines but not in lymyb. We also showed that heat and osmotic stress activate the NIK1/RPL10/LIMYB signaling circuit readouts in wild-type lines. The coordinated repression of photosynthesis and translation via the NIK1/RPL10/LIMYB signaling module indicates how viruses and abiotic signals coordinately regulate these opposing energy-producing and consuming processes.