Modulation of host plant immunity by Tobamovirus proteins

Abstract

Background: To establish successful infection, plant viruses produce profound alterations of host physiology, disturbing unrelated endogenous processes and contributing to the development of disease. In tobamoviruses, emerging evidence suggests that viral-encoded proteins display a great variety of functions beyond the canonical roles required for virus structure and replication. Among these, their modulation of host immunity appears to be relevant in infection progression.

Scope: In this review, some recently described effects on host plant physiology of Tobacco mosaic virus (TMV)-encoded proteins, namely replicase, movement protein (MP) and coat protein (CP), are summarized. The discussion is focused on the effects of each viral component on the modulation of host defense responses, through mechanisms involving hormonal imbalance, innate immunity modulation and antiviral RNA silencing. These effects are described taking into consideration the differential spatial distribution and temporality of viral proteins during the dynamic process of replication and spread of the virus.

Conclusion: In discussion of these mechanisms, it is shown that both individual and combined effects of viral-encoded proteins contribute to the development of the pathogenesis process, with the host plant's ability to control infection to some extent potentially advantageous to the invading virus.

Keywords: DELLA proteins; RNA silencing; Tobacco mosaic virus; coat protein; immune response; movement protein; reactive oxygen species; replicase; salicylic acid.

Fig. 1.

Schematic view of the proposed events associated with the replication and movement of TMV. (A) The early stage of the infection is determined by the entry of a viral particle into the symplast of a single cell, the disassembly of the virions and translation of the 126 and 183 kDa subunits of the replicase. Subsequently, negative strands and sub-genomic RNAs are synthesized to produce first the MP and then the CP. The accumulation of positive stranded viral RNAs and CPs permit the assembly of new viral particles. (B) The intermediate stages of infection are determined by the local spread of the viral RNAs between adjacent cells. The MP is implicated in facilitating the transport due to its ability to interact with plasmodesmata and bind RNA. (C) The late stages of infection are initiated when the virus reaches distant parts of the plants through vascular tissues and the infection becomes systemic. The systemic virus movement is facilitated by the CP by an incompletely understood mechanism. At this stage, the newly assembled viral particles can invade other plants by direct transmission.

Fig. 2.

Dynamic overview of plant immunity modulation mechanisms mediated by the different TMV proteins. (A) In the single-cell early stages of the infection, the uncoating of the viral RNA (viral PAMP) triggers the activation of RNA silencing as a first barrier of antiviral defence (antiviral PTI). The replicase is the first viral protein to be translated and presents silencing suppression activity (viral ETS). In the bottom of this panel, a representative zig–zag model is shown. (B) At intermediate stages of the infection, the MP initiates accumulation and allows the virus to invade adjacent cells by facilitating passage through plasmodesmata. The MP is detected by the host and activates immune defences, thus triggering an antiviral ETI response. It acts as a defence elicitor mediated by induction of ROS and SA accumulation, induction of SA-responsive genes and downregulation of ROS-scavenging genes. It also acts as an enhancer of RNA silencing, mediating the facilitation of vsiRNAs transport across plasmodesmata. In the bottom of the figure, a representative zig–zag model is shown. (C) During late stages of infection, the CP becomes the more abundant viral protein accumulated in the infected cells. The CP is involved in the systemic movement, permits the assembly of new viral particles and is implicated in the negative modulation of host immunity, giving rise to a new round of viral ETS. The suppression of SA-mediated defence responses by the CP is triggered by the downregulation of SA-responsive genes via the stabilization of DELLA proteins. In the bottom of the figure, a representative zig–zag model is shown.