Intracellular coordination of potyviral RNA functions in infection

Abstract

Establishment of an infection cycle requires mechanisms to allocate the genomes of (+)-stranded RNA viruses in a balanced ratio to translation, replication, encapsidation, and movement, as well as mechanisms to prevent translocation of viral RNA (vRNA) to cellular RNA degradation pathways. The ratio of vRNA allocated to various functions is likely balanced by the availability of regulatory proteins or competition of the interaction sites within regulatory ribonucleoprotein complexes. Due to the transient nature of viral processes and the interdependency between vRNA pathways, it is technically demanding to work out the exact molecular mechanisms underlying vRNA regulation. A substantial number of viral and host proteins have been identified that facilitate the steps that lead to the assembly of a functional potyviral RNA replication complex and their fusion with chloroplasts. Simultaneously with on-going viral replication, part of the replicated potyviral RNA enters movement pathways. Although not much is known about the processes of potyviral RNA release from viral replication complexes, the molecular interactions involved in these processes determine the fate of the replicated vRNA. Some viral and host cell proteins have been described that direct replicated potyviral RNA to translation to enable potyviral gene expression and productive infection. The antiviral defense of the cell causes vRNA degradation by RNA silencing. We hypothesize that also plant pathways involved in mRNA decay may have a role in the coordination of potyviral RNA expression. In this review, we discuss the roles of different potyviral and host proteins in the coordination of various potyviral RNA functions.

Keywords: potyviral RNA degradation; potyviral RNA encapsidation; potyviral RNA functions; potyviral movement; potyviral replication; potyviral translation; potyviruses.

FIGURE 1

Viral RNA pathways in infected cell. In a newly infected cell, polysomes translate viral RNA (vRNA, pathway 1), and it is recruited to VRCs (pathway 2). The replicated vRNA is transported to plasmodesmata to facilitate cell-to-cell movement (pathway 3). To achieve productive infection, vRNA expression continues via new rounds of translation/replication (pathway 4). Host cell defense mechanisms leading to RNA degradation actively compete for vRNA substrates with viral counterdefense mechanisms (pathway 5). vRNA encapsidation completes the infection cycle (pathway 6), allowing the encapsidated virus to be transported and infect neighboring healthy plants.

FIGURE 2

A model of interdependent targeting of potyviral RNA in translation and movement. This model of interdependency between vRNA targeting either in translation or movement is based on the observation that VPg, when abundantly present in infected cells, targets vRNA in translation, which is accompanied by a reduction in viral cell-to-cell movement (Hafrén et al., 2013).

FIGURE 3

A model of a virus-specific mechanism to boost viral RNA translation. P0 transcription is induced in PVY and PVA infection (Baebler et al., 2009; Vuorinen et al., 2010 ) and TuMV infection upregulates eIF4E (Léonard et al., 2004), suggesting that the demand for these proteins is increased during natural potyvirus infection. VPg, eIF4E/(iso)4E, and P0 enhance PVA RNA expression (Hafrén et al., 2013), resulting in the production of a large amount of viral proteins, e.g., CP required for virion assembly at later stages of infection.

FIGURE 4

Viral RNA stability is determined by host antiviral activity and the success of viral counterdefence. Potyviral RNA may be subjected to degradation by RNA silencing, RNase activity of the ubiquitin-proteasome system, and, as suggested here, mRNA decay pathways unless rescued by viral counterdefense mechanisms. Many links may exist between the RNA degradation pathways. The manner in which vRNA combats viral counterdefense mechanisms and is returned to the active translation/replication pathway (dashed line arrow) is unknown.