Three-Dimensional Architecture and Biogenesis of Membrane Structures Associated with Plant Virus Replication

Abstract

Positive-sense (+) RNA viruses represent the most abundant group of viruses and are dependent on the host cell machinery to replicate. One remarkable feature that occurs after (+) RNA virus entry into cells is the remodeling of host endomembranes, leading to the formation of viral replication factories. Recently, rapid progress in three-dimensional (3D) imaging technologies, such as electron tomography (ET) and focused ion beam-scanning electron microscopy (FIB-SEM), has enabled researchers to visualize the novel membrane structures induced by viruses at high resolution. These 3D imaging technologies provide new mechanistic insights into the viral infection cycle. In this review, we summarize the latest reports on the cellular remodeling that occurs during plant virus infection; in particular, we focus on studies that provide 3D architectural information on viral replication factories. We also outline the mechanisms underlying the formation of these membranous structures and discuss possible future research directions.

Keywords: biogenesis; cellular remodeling; plant virus; three-dimensional architecture; viral replication factories.

Figure 1

BBSV remodels ER membranes and 3D model of BBSV-induced vesicle packets. (A) BBSV infection led to ER aggregation and vesiculation. (B) Vesicle packets were observed in the aggregates of branched ER cisternae (star). (C,D) Slices from the electron tomogram of BBSV-induced vesicle packets and spherules derived from ER. Arrowheads indicate the same spherules in different slices. The spherules are connected to the outer ER membrane. (E) Three-dimensional model of BBSV-induced vesicle packets and spherules derived from ER. Vi, virus particles or virus crystals; Va, vacuole; gold, vesicle packet derived from ER outer membrane; gray, spherules; green, fibrillar materials within the spherules. This figure is adapted with permission from Cao et al. (2015) (© 2015 by the American Society for Microbiology).

Figure 2

3D reconstruction of the TBSV replication platform in yeast. (A) 3D model of the TBSV replication platform in wild-type yeast cells characterized by peroxisome peripheral MVBs. Yellow, peripheral MVB membranes; blue, vesicle-like spherules; red, a mitochondrion. (B) 3D model of TBSV replication platform in Δpah1 yeast cells characterized by a large membrane compartment (asterisk) containing MVB-like structures with spherules and stacked ER. Yellow, stacked ER membranes; blue, spherules. This figure is adapted with permission from Fernández de Castro et al. (2017) (© 2017 by the Company of Biologists).

Figure 3

TEM analysis and 3D reconstruction of MNSV-induced altered mitochondria. (A) TEM image showing altered mitochondria. Numerous vesicles were observed on the external surface as well as internal large invaginations and internal dilations (star), or both. Yellow arrowheads indicate the pores connecting the lumen of the dilation to the surrounding cytoplasm. (B) 3D model of MNSV-induced altered mitochondria with large dilations inside analyzed by FIB-FESEM. Connections between different mitochondria as well as with lipid bodies are observed. Blue, yellow, red, and purple indicate altered mitochondria; chloroplasts are shown in green and lipid bodies in gray. This figure is adapted with permission from Gómezaix et al. (2015) (© 2015 by the American Phytopathological Society).

Figure 4

3D reconstruction of TuMV-induced SMTs at midstage of infection. (A) Tomogram slice from TuMV-infected vascular parenchymal cell. SMVL structures are seen in close proximity to dilated rER. (B) 3D surface rendering of TuMV-induced SMTs that connect with the rough ER. Yellow, SMTs; sky blue, rough ER; magenta, cytoplasmic inclusion body; red arrows, connection between the rough ER membrane and an SMT. (C) 3D model of the SMT with fibrillar materials inside. Yellow, SMTs; light red, electron-dense materials; green, intermediate tubular structures. This figure is adapted with permission from Wan et al. (2015) (© 2015 by the American Society for Microbiology).

Figure 5

BSMV-induced chloroplast membrane rearrangement and 3D model of altered chloroplast membranes. (A,B) Tomogram slices of altered chloroplast membranes from leaves of BSMV-infected N. benthamiana. The arrowheads indicate the same spherules in different slices. (C) 3D model of remodeled chloroplast membranes induced by BSMV. Light blue, outer chloroplast membrane (OM); translucent white, inner chloroplast membrane (IM); light yellow, spherules derived from the outer membrane. (D) Representative tomogram slice of remodeled chloroplast in BSMV-infected N. benthamiana leaves by FIB-SEM. The arrowhead indicates the opening of a CI. (E) 3D visualization by FIB-SEM of a chloroplast in a BSMV-infected cell. Chl, chloroplast; CI, cytoplasmic invagination; green, chloroplast; yellow, CI; white arrowheads, chloroplast invaginations; black arrow, CI aperture. The inset shows an enlarged view of a CI. This figure is adapted with permission from Jin et al. (2018) (© 2018 by the American Society of Plant Biologists).