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Review
. 2016 Aug 18;8(8):228.
doi: 10.3390/v8080228.

Ins and Outs of Multipartite Positive-Strand RNA Plant Viruses: Packaging versus Systemic Spread

Mattia Dall'Ara  1   2 , Claudio Ratti  3 , Salah E Bouzoubaa  4 , David Gilmer  5
Affiliations
Review

Ins and Outs of Multipartite Positive-Strand RNA Plant Viruses: Packaging versus Systemic Spread

Mattia Dall'Ara et al. Viruses. .

Abstract

Viruses possessing a non-segmented genome require a specific recognition of their nucleic acid to ensure its protection in a capsid. A similar feature exists for viruses having a segmented genome, usually consisting of viral genomic segments joined together into one viral entity. While this appears as a rule for animal viruses, the majority of segmented plant viruses package their genomic segments individually. To ensure a productive infection, all viral particles and thereby all segments have to be present in the same cell. Progression of the virus within the plant requires as well a concerted genome preservation to avoid loss of function. In this review, we will discuss the "life aspects" of chosen phytoviruses and argue for the existence of RNA-RNA interactions that drive the preservation of viral genome integrity while the virus progresses in the plant.

Keywords: RNA-RNA interaction; genome integrity; phytovirus; segmented genome; systemic movement.

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Figures

Figure 1
Figure 1
Schematic representation of the initial infection (red thunderbolt) and its progression (red lines and arrows) within a source leaf of an infected plant. Infectious material passes through plasmodesmata (Pd, double green ovals) from mesophyll (ME), bundle sheath (BS), vascular parenchyma (VP) to companion cells (CC) to access sieve elements (SE) and reach the distant tissues. A reverse route occurs in the upper leaves (sink leaf) or roots (not represented). Right panels show leaf venation and illustrate viral phloem loading and unloading through minor and major veins of source and sink leaves. X, Xyleme; I−V: vein classes.
Figure 2
Figure 2
Simplified representation of replication cycle and movement of Beet necrotic yellow vein virus (BNYVV) used as model. The four genomic RNAs of the segmented helical virus (1) are expressed and amplified (2). On this scheme the RNA-RNA interaction network between genomic segments (3 and 4), stabilized by viral proteins, allows the preservation of genome integrity during long-distance movement (5) in the sieve elements (blue shaded). In particular the presence of the coat protein (CP) and the viral suppressors of RNA silencing (VSR) is necessary for their systemic movement. Vice versa the genomic RNAs can move cell to cell without the need of the CP expression but require triple gene block (TGB) movement proteins (6). ER: endoplasmic reticulum; CP-RT: coat protein-readthrough; N: Nucleus; RdRp: RNA-dependent RNA polymerase.
Figure 3
Figure 3
Confrontation of two models describing the long-distance movement of multipartite RNA viruses using the BNYVV as an example. The bottom of the graphic represents the progression of an initial infection of mesophyll cells, wherein the infection progresses thanks to the individual cell-to-cell movement of viral RNAs, driven by TGB movement proteins (1) or as ribonucleoprotein (RNP) complexes involving RNA-RNA network between genomic segments (2). In the sieve elements (blue), the virion (3) or the RNP complexes (4) are transported through plasmodesmata thanks to the viral proteins. RNP complexes, driving the export of the viral genomic RNA network, could provide each distant cell with an entire and fully functional genome (5). Virions (or single viral RNAs, not presented) are transported in the sieve elements and are randomly distributed in the distant cells (6). Only the combination providing one of each viral particle (or RNA) is able to initiate an infection that preserves the genome integrity (7). The particles (or RNA) entering cells without the entire genome are either deficient for replication (not shown) or unable to move from cell to cell and express the VSR, leading to the trigger of RNA silencing (8).
Figure 4
Figure 4
Fluorescence profile of a C. quinoa local lesion observed 7 days post infection after rub-inoculation of BNYVV RNA1 and RNA2 supplemented with a mixture of two replicons derived from BSBMV and BNYVV RNA3s, expressing monomeric red fluorescent protein (mRFP) and enhanced green fluorescent protein (EGFP), respectively. This image illustrates the existence of an exclusion mechanism for similar but distinct RNA species during the progression of the infection, with both replicons being able to be encapsidated by BNYVV CP (details are described in Ratti et al., 2009 [104]).
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