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Review
. 2017 Sep 27:8:1672.
doi: 10.3389/fpls.2017.01672. eCollection 2017.

Inspirations on Virus Replication and Cell-to-Cell Movement from Studies Examining the Cytopathology Induced by Lettuce infectious yellows virus in Plant Cells

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Review

Inspirations on Virus Replication and Cell-to-Cell Movement from Studies Examining the Cytopathology Induced by Lettuce infectious yellows virus in Plant Cells

Wenjie Qiao et al. Front Plant Sci. .

Abstract

Lettuce infectious yellows virus (LIYV) is the type member of the genus Crinivirus in the family Closteroviridae. Like many other positive-strand RNA viruses, LIYV infections induce a number of cytopathic changes in plant cells, of which the two most characteristic are: Beet yellows virus-type inclusion bodies composed of vesicles derived from cytoplasmic membranes; and conical plasmalemma deposits (PLDs) located at the plasmalemma over plasmodesmata pit fields. The former are not only found in various closterovirus infections, but similar structures are known as 'viral factories' or viroplasms in cells infected with diverse types of animal and plant viruses. These are generally sites of virus replication, virion assembly and in some cases are involved in cell-to-cell transport. By contrast, PLDs induced by the LIYV-encoded P26 non-virion protein are not involved in replication but are speculated to have roles in virus intercellular movement. These deposits often harbor LIYV virions arranged to be perpendicular to the plasma membrane over plasmodesmata, and our recent studies show that P26 is required for LIYV systemic plant infection. The functional mechanism of how LIYV P26 facilitates intercellular movement remains unclear, however, research on other plant viruses provides some insights on the possible ways of viral intercellular movement through targeting and modifying plasmodesmata via interactions between plant cellular components and viral-encoded factors. In summary, beginning with LIYV, we review the studies that have uncovered the biological determinants giving rise to these cytopathological effects and their importance in viral replication, virion assembly and intercellular movement during the plant infection by closteroviruses, and compare these findings with those for other positive-strand RNA viruses.

Keywords: Closteroviridae; cytopathology; intercellular movement; membrane remodeling; plasmodesmata; virus replication.

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Figures

FIGURE 1
FIGURE 1
Schematic diagrams of the genome structure of the representative viruses in the four genera of the family Closteroviridae. LIYV, Lettuce infectious yellows virus, genus Crinivirus; BYV, Beet yellows virus, genus Closterovirus; GLRaV-3, Grapevine leafroll-associated virus 3, genus Ampelovirus; GLRaV-7, Grapevine leafroll-associated virus 7, genus Velarivirus. ORFs are shown as boxes, with the related domains indicated in the same in-fill. PRO, papain-like cysteine proteinase; MTR, methyltransferase; HEL, helicase; POL, RNA-dependent RNA polymerase; HSP70h, heat shock protein 70 homolog; CP, capsid protein; CPm, minor capsid protein; P, proteins named by their approximate molecular mass (e.g., P34, 34-kDa protein). The functional roles of some of the protein products are indicated with the well-studied LIYV and BYV. Genome size is labeled on the right side.
FIGURE 2
FIGURE 2
Transmission electron micrographs showing LIYV-induced conical plasmalemma deposits (PLDs). (A) Shows PLDs located at the internal side in a companion cell (CC) of a LIYV-infected Nicotiana benthamiana leaf, associated with LIYV virions (V) and plasmodesmata (P) [image is modified from Medina et al. (2003) with permission of John Wiley and Sons]. (B) Shows PLDs in a LIYV-infected N. benthamiana protoplast, sacks of LIYV virions (V) are external to the plasmalemma directly adjacent to abundant PLDs [image is modified from Kiss et al. (2013) under the CC BY License]. Labeling is CC, companion cell; P, plasmodesmata; PLD, plasmalemma deposit; SE, sieve element; V, LIYV virions.
FIGURE 3
FIGURE 3
Virus-induced membrane modification. (A) 3D architecture of HCV-induced membrane rearrangements. HCV DMVs are protrusions from the ER membrane into the cytosol. The enlarged DMV structure displays a connection between the outer membrane of a DMV and the ER membrane (red arrow) and a pore-like opening that connects the interior of the DMV with the cytosol (blue arrow). (B) ET and 3D reconstruction of TuMV-induced membrane rearrangement. SMVs (yellow) are in close proximity or connected (red arrows) to dilated rER (sky blue). (C) ET and 3D reconstruction of FHV-induced spherule rearrangements of a mitochondrion. Numerous spherules (white) are shown as outer mitochondrial membrane (OM, blue) invaginations with interiors connected to the cytoplasm by a necked structure (arrows). IM, inner mitochondrial membrane. (D) ET and 3D model of BBSV-induced membrane rearrangements. Spherules (gray) are shown within ER-derived vesicle packets (indicated by I, II, III) and are connected to the ER outer membrane (gold) through neck-like structures (arrows). Green, fibrillar materials inside the spherules. (A) is adapted from Romero-Brey et al. (2012) under the CC BY License; (B) is adapted from Wan et al. (2015a) with permission of the American Society for Microbiology; (C) is adapted from Kopek et al. (2007) under the CC BY License; (D) is adapted from Cao et al. (2015) with permission of the American Society for Microbiology.

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