Activation of the NIK1/RPL10/LIMYB signaling circuit by biotic and abiotic signals and regulation of defense and growth parameters
Authors:   , Teixeira Ruan Maloni 
Published: August 2022

Plants are constantly exposed to different microorganisms such as viral pathogens. Geminiviruses are circular DNA viruses encapsidated in geminate virion particles, which infect many crops and cause significant agricultural restrictions. Geminiviruses developed strategies to evade a potent plant antiviral immune system maintaining their broad spectrum of hosts and establishing successful infections. For this, it is necessary that these viruses overcome a multilayered perception system represented by RNA interference sensors and effectors, pattern recognition receptors (PRR) and resistance proteins (R). This recognition system leads to the activation of conserved defense responses that protect plants against different viral and non-viral pathogens existing in nature. Furthermore, a specific antiviral cell surface receptor signaling is activated early in geminivirus infection to suppress global translation. In this investigation, we first presented a review of the layers of virus perception and host defenses and the mechanisms developed by geminiviruses to overcome the plant's antiviral immunity mechanisms. Plant immunity depends on recognition of viral components or effectors by host receptors. This system is composed of two defense layers; the first one occurs from the recognition of molecular patterns associated with pathogens (PAMPs), designated PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI). Emerging evidence in the literature has included classic PTI in the innate antiviral immune arsenal of plant cells. Therefore, our understanding of PAMPs has expanded to include not only classical PAMPs such as bacterial flagellin or fungal chitin, but also virus-derived nucleic acids that can also activate PAMP recognition receptors as documented for mammalian viruses. In our second review, we discussed the understanding that plant viruses can activate classical PTI, leading to both unique antiviral responses and conserved responses to pathogens. We also present evidence that PAMPs derived from viral nucleic acids can trigger the NUCLEAR SHUTTLE PROTEIN-INTERACTING KINASE 1 (NIK1)-mediated antiviral immunity. The NIK1 immune pathway is initiated after perception that leads to receptor phosphorylation, triggering a signaling cascade that phosphorylates the ribosomal protein L10 (RPL10), which is translocated to the nucleus and interacts with the factor L10- INTERACTING MYB DOMAIN-CONTAINING PROTEIN (LIMYB) to suppress host global translation. Transcriptome studies by overexpressing LIMYB in Arabidopsis also demonstrated that LIMYB, in addition to translation-related genes, represses the expression of photosynthetic apparatus-related genes. Photosynthesis and translation are targets of metabolic control and development in plants; however, how stress signals coordinately regulate these opposing energy production and consumption processes remains enigmatic. Here, we delineate a growth control circuit that links photosynthetic function to translational control in response to biotic and abiotic signals. We first showed that the downstream component of the NIK1/RPL10 antiviral signaling circuit, LIMYB, which represses the expression of translation machinery-related genes, also represses the expression of transcriptional repression activity of LIMYB was the main determinant for the decrease in electron transport rate, gas exchange parameters, quantum efficiency and water use efficiency in the LIMYB-ectopic expressing lines. Decreased photosynthetic activity was linked to NIK1 antiviral signaling and stunted growth. NIK1 activation by viral or bacterial PAMPs, or by expressing a constitutively activated NIK1mutant, T474D, inhibited photosynthetic function in control lines, but not in limyb knockout plants. We have also shown that heat and osmotic stress activate the NIK1/RPL10/LIMYB signaling circuit. Coordinated inhibition of photosynthesis and translation via the stress-activated NIK1/RPL10/LIMYB signaling module can adjust the plant's growth pattern in response to the changing environment. Finally, the RNA-seq and ChIP-seq analyses also defined a set of genes upregulated by LIMYB. Among them, phenylpropanoid biosynthesis genes were remarkably enriched. NIK1 activation by begomovirus-derived nucleic acids induced genes involved in lignin synthesis. As a result, the transgenic lines LIMYB and T474D displayed higher lignin content than the control lines. As a plant defense mechanism, the attack by pathogens leads to the thickening of the cell wall by lignification to prevent the entry of microorganisms, a process typically controlled by MYB- type transcription factors. Consequently, the results of this investigation extended the transcriptional function of LIMYB, demonstrating that it also targets photosynthesis and lignin synthesis. They indicated that the NIK1/RPL10/LIMYB signaling module, initially described as an antiviral signal transducer, controls plant growth under biotic and abiotic stress conditions and may also define another layer of defense against non-viral pathogens via lignin accumulation. Keywords: Molecular Biology. Plants. Transcriptome. LIMYB. plant immunity. viral PAMPs. NIK1. Heat Stress. Osmotic Stress. Phenylpropanoids. Lignin Synthesis.