Translational control in plant antiviral immunity

Abstract

Due to the limited coding capacity of viral genomes, plant viruses depend extensively on the host cell machinery to support the viral life cycle and, thereby, interact with a large number of host proteins during infection. Within this context, as plant viruses do not harbor translation-required components, they have developed several strategies to subvert the host protein synthesis machinery to produce rapidly and efficiently the viral proteins. As a countermeasure against infection, plants have evolved defense mechanisms that impair viral infections. Among them, the host-mediated translational suppression has been characterized as an efficient mean to restrict infection. To specifically suppress translation of viral mRNAs, plants can deploy susceptible recessive resistance genes, which encode translation initiation factors from the eIF4E and eIF4G family and are required for viral mRNA translation and multiplication. Additionally, recent evidence has demonstrated that, alternatively to the cleavage of viral RNA targets, host cells can suppress viral protein translation to silence viral RNA. Finally, a novel strategy of plant antiviral defense based on suppression of host global translation, which is mediated by the transmembrane immune receptor NIK1 (nuclear shuttle protein (NSP)-Interacting Kinase1), is discussed in this review.

Virus perception at the cell surface: revisiting the roles of receptor‐like kinases as viral pattern recognition receptors

“…Although NIK1 is structurally related to SERKs and is also implicated in plant immunity, the mechanism by which NIK1 propagates an antiviral signal, and the resulting immune responses are entirely different from the BAK1/SERK3‐dependent PTI response against pathogens (Machado et al , ). The mechanism of NIK1‐mediated defence is underscored by repression of translational machinery genes and suppression of global translation, as a new paradigm for plant antiviral immunity (Machado et al , ; Zorzatto et al , ).…”

Proteome-wide Profiling of RNA-Binding Protein Responses to flg22 Reveals Novel Components of Plant Immunity

“…Hence, our data provides further insights into translation regulation during plant immunity, showing that the RNA-binding activity of multiple components of the translation machinery, including ribosomal proteins, is altered in response to flg22. A similar global translational slowdown has been suggested to play important roles as an antiviral strategy 37 and to occur during responses to abiotic stresses such as hypoxia 38 , heat 39 or drought 40 . We hypothesise that this phenomenon may play a role in or be a consequence of the described switch from translation of growthrelated mRNAs to those involved in rapid adaptive responses 36 .…”

A Begomovirus Nuclear Shuttle Protein-Interacting Immune Hub: Hijacking Host Transport Activities and Suppressing Incompatible Functions

“…The mechanistic model for NIK1 activation and defense assembly holds that, in response to virus infection, begomovirusderived nucleic acids function as PAMPs to mediate dimerization of NIK1 with itself, its paralog NIK2 or another unknown transmembrane receptor, which may function as a PAMP recognition receptor (PRR) (Teixeira et al, 2019). The NIK1 oligomerization induces the phosphorylation of the NIK1 kinase domain at the key threonine residue at position 474 (Machado et al, 2015(Machado et al, , 2017. This phosphorylation-induced activation of NIK1 mediates the phosphorylation of the downstream component RPL10, which, in turn, is reallocated from the cytoplasm to the nucleus, where it binds to LIMYB.…”

“…Likewise, the binding of NSP to defense proteins, such as NIK1 and AS2, leads to suppression of host immunity. In the first case, during infection, NSP inhibits the NIK1 kinase that otherwise would transduce an antiviral signal to protect plants against begomoviruses (Brustolini et al, 2015;Machado et al, 2015Machado et al, , 2017. In the latter case, NSP not only increases AS2 expression, an endogenous suppressor of PTGS, but also can induce nuclear export of AS2 to the cytosol where it interacts with DCP2 to stimulate decapping activity, decrease siRNA accumulation and impair RNA silencing (Ye et al, 2015).…”