NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism

Abstract

Plants and plant pathogens are subject to continuous co-evolutionary pressure for dominance, and the outcomes of these interactions can substantially impact agriculture and food security1–3. In virus– plant interactions, one of the major mechanisms for plant antiviral immunity relies on RNA silencing, which is often suppressed by co-evolving virus suppressors, thus enhancing viral pathogenicity in susceptible hosts1. In addition, plants use the nucleotide-binding and leucine-rich repeat (NB-LRR) domain-containing resistance proteins, which recognize viral effectors to activate effector-triggered immunity in a defence mechanism similar to that employed in non-viral infections2,3. Unlike most eukaryotic organisms, plants are not known to activate mechanisms of host global translation suppression to fight viruses1,2. Here we demonstrate in Arabidopsis that the constitutive activation of NIK1, a leucine-rich repeat receptor-like kinase (LRR-RLK) identified as a virulence target of the begomovirus nuclear shuttle protein (NSP)4–6, leads to global translation suppression and translocation of the downstream component RPL10 to the nucleus, where it interacts with a newly identified MYB-like protein, L10-INTERACTING MYB DOMAIN-CONTAINING PROTEIN (LIMYB), to downregulate translational machinery genes fully. LIMYB overexpression represses ribosomal protein genes at the transcriptional level, resulting in protein synthesis inhibition, decreased viral messenger RNA association with polysome fractions and enhanced tolerance to begomovirus. By contrast, the loss of LIMYB function releases the repression of translation-related genes and increases susceptibility to virus infection. Therefore, LIMYB links immune receptor LRR-RLK activation to global translation suppression as an antiviral immunity strategy in plants.

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

“…Total nucleic acids were extracted from systemically infected leaves using a cetyltrimethylammonium bromide (CTAB)-based method (63). Viral DNA accumulation was measured using qPCR as described previously (26). Relative viral DNA accumulation levels were calculated by the comparative threshold cycle (C T ) method (64).…”

“…Recently, R gene-mediated resistance has been proposed as another essential defense strategy against geminiviruses. For example, the begomovirus nuclear shuttle protein (NSP)-interacting kinase 1 (NIK1) is able to activate antiviral immunity against cabbage leaf curl virus (CaLCuV) (25,26). Besides the above-mentioned defense mechanisms, host factors such as SNF1-related protein kinase 1 (SnRK1) have also been involved in defense against geminiviruses (27)(28)(29).…”

rgs-CaM Detects and Counteracts Viral RNA Silencing Suppressors in Plant Immune Priming

“…Another class of receptors, NB-LRRs, counteractively recognize pathogen effector proteins and induce strong defense reactions, called hypersensitive responses; this mechanism is termed effector-triggered immunity (ETI) (50,51). Several NB-LRRs that perceive virus invasion and induce ETI have been identified (52), and recent studies of Arabidopsis RLKs (53,54) suggest the existence of an immune receptor that perceives dsRNAs or other viral factors as viral PAMPs and induces PTI. In animals, Toll-interleukin 1-like receptors (TLRs), which are structurally similar to plant RLKs and NB-LRRs, perceive viral RNA and DNA in endosomes and on cell membranes (55).…”

Plant immunity against viruses: antiviral immune receptors in focus

“…In order to gain new insights into the molecular mechanisms of NIK1 in antiviral immunity, arabidopsis transgenic lines harbouring the gain-of-function mutant T474D on a nik1 knockout background were analysed for gene expression (Zorzatto et al, 2015). The constitutive activation of NIK-mediated signalling resulted in the down-regulation of translation-related genes and the suppression of global translation, decreasing the loading of host mRNAs in actively translating polysomes (Zorzatto et al, 2015).…”

“…Plants have also been found to use innate pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) to limit viral infection (Kørner et al, 2013). More recently, a transmembrane immune receptor, which is structurally similar to co-receptor-like kinases involved in PTI, has been shown to activate host translation suppression to fight DNA viruses, a newly discovered mechanism for antiviral defences in plants (Zorzatto et al, 2015). Viral infections can also lead to hormonal disruption, which manifests as simultaneous induction of many antagonistic hormones and triggering of defence responses (Alazem and Lin, 2015).…”