Fontes, E. P. B. | bioRxiv Science

bioRxiv2023

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

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.

plant biology↗

bioRxiv2020

A new plant-specific syntaxin-6 protein may define an intracytoplasmic route for begomoviruses

Due to limited free diffusion in the cytoplasm, viruses must use active transport mechanisms to move intracellularly. Nevertheless, how the plant ssDNA begomoviruses hijacks the host intracytoplasmic transport machinery to move from the nucleus to the plasmodesmata remains enigmatic. Here, we identified nuclear shuttle protein (NSP)-interacting proteins from Arabidopsis by probing a protein microarray and demonstrated that the Cabbage leaf curl virus (CabLCV) NSP, a facilitator of the nucleocytoplasmic trafficking of viral (v)DNA, interacts with an endosomal vesicle-localized plant-specific syntaxin-6 protein, designated NSP-interacting syntaxin-6 domain-containing protein (NISP) in planta. NISP displays a pro-viral function, but not the syntaxin-6 paralog AT2G18860 that failed to interact with NSP. Consistent with these findings, nisp-1 mutant plants were less susceptible to begomovirus infection, a phenotype reversed by NISP complementation. NISP-overexpressing lines accumulated higher levels of viral DNA than wild-type. Furthermore, NISP interacted with NIG, an NSP-interacting GTPase involved in NSP-vDNA nucleocytoplasmic translocation. The NISP-NIG interaction was enhanced by NSP. We also showed that NISP associates with vDNA and might assemble a NISP-NIG-NSP-vDNA-complex. NISP may function as a docking site for recruiting NIG and NSP into endosomes, providing a mechanism for the intracytoplasmic translocation of the NSP-vDNA complex towards to and from the cell periphery.Author Summary As viruses must use an active and directed intracellular movement, they hijack the intracellular host transport system for their own benefits. Therefore, the identification of interactions between host proteins and begomovirus movement proteins should target the intracellular transport machinery. This work focused on the identification of these protein-protein interactions; it addressed the molecular bases for the intracellular transport of begomoviruses. We used a protein microarray to identify cellular partners for the movement protein (MP) and the viral nuclear shuttle protein (NSP), which is a facilitator of the nucleocytoplasmic trafficking of viral (v)DNA. We identified relevant protein-protein interaction (PPI) hubs connecting host and viral proteins. We revealed a novel NSP-interacting protein, which functions in the intracytoplasmic transport of proteins and DNA from begomoviruses and was designated NSP-interacting syntaxin domain-containing protein (NISP). Our data suggest an intracellular route connecting the release of newly synthesized begomoviral DNA in the cytosol with the cell surface. Resolving viral DNA-host protein complexes led to the identification of a novel class of components of the cell machinery and a representative member, NISP, that functions as a susceptibility gene against begomoviruses. As geminiviruses pose a severe threat to agriculture and food security, this recessive gene can now be exploited as a target for engineering resistance by gene editing in crops.Competing Interest StatementThe authors have declared no competing interest.View Full Text

plant biology↗