Coordinated regulation of photosynthesis and translation via NIK1/RPL10/LIMYB signaling module in response to biotic and abiotic stresses

Abstract

Photosynthesis and translation are targets of metabolic control and development in plants, yet, how stress signals coordinately regulate these opposing energy-producing and consuming processes remains enigmatic. Here, we described a growth control circuit that ties the photosynthetic function to translational control in response to biotic and abiotic signals. We showed first 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 repressing transcriptional 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 or bacterial 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. Conversely, in limyb-32 knockout, heat and osmotic stress induced NIK1 phosphorylation but did not cause repression of the marker genes, indicating that LIMYB links NIK1 activation to the stress-mediated downregulation of translation- and photosynthesis-related genes. The coordinated repression of photosynthesis and translation via the stress-activated NIK1/RPL10/LIMYB signaling module may adjust the plant growth pattern in response to the changing environment. Short summaryThe receptor-like kinase NIK1 (NSP-Interacting Kinase 1) undergoes phosphorylation under multiple biotic and abiotic signals activating the NIK1/RPL10/LIMYB signaling circuit, which coordinately downregulates translation and photosynthesis in response to the changing environment.