AFM Study of Potato Virus X Disassembly Induced by Movement Protein

Kiselyova, Olga I.; Яминский, И.В.; Карпова, О. В.; Родионова, Н. В.; Kozlovsky, Stanislav V.; Arkhipenko, M. V.; Atabekov, J.G.

doi:10.1016/s0022-2836(03)00835-0

Cited by 61 publications

(55 citation statements)

References 13 publications

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“…One side is represented by potexviruses, where TGBp1 contains no N-terminal extension region and the CP is essential for both cell-to-cell and long-distance transport (Beck et al, 1991;Chapman et al, 1992). It is assumed that virions rather than viral RNA or a viral RNP complex is the transport form of the virus genome (Santa Cruz et al, 1998;Morozov & Solovyev, 2003), which is in agreement with the discovery of specific complexes between TGBp1 and potexvirus virions (Atabekov et al, 2000;Kiselyova et al, 2003;Rodionova et al, 2003;Karpova et al, 2006). The opposite pole is occupied by hordeiviruses characterized by the longest known TGBp1 N-terminal extension region.…”

Section: Discussionsupporting

confidence: 62%

Domain organization of the N-terminal portion of hordeivirus movement protein TGBp1

Makarov

Rybakova

Ефимов

et al. 2009

Journal of General Virology

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Three 'triple gene block' proteins known as TGBp1, TGBp2 and TGBp3 are required for cell-tocell movement of plant viruses belonging to a number of genera including Hordeivirus. Hordeiviral TGBp1 interacts with viral genomic RNAs to form ribonucleoprotein (RNP) complexes competent for translocation between cells through plasmodesmata and over long distances via the phloem. Binding of hordeivirus TGBp1 to RNA involves two protein regions, the C-terminal NTPase/ helicase domain and the N-terminal extension region. This study demonstrated that the extension region of hordeivirus TGBp1 consists of two structurally and functionally distinct domains called the N-terminal domain (NTD) and the internal domain (ID). In agreement with secondary structure predictions, analysis of circular dichroism spectra of the isolated NTD and ID demonstrated that the NTD represents a natively unfolded protein domain, whereas the ID has a pronounced secondary structure. Both the NTD and ID were able to bind ssRNA non-specifically. However, whilst the NTD interacted with ssRNA non-cooperatively, the ID bound ssRNA in a cooperative manner. Additionally, both domains bound dsRNA. The NTD and ID formed low-molecular-mass oligomers, whereas the ID also gave rise to high-molecular-mass complexes. The isolated ID was able to interact with both the NTD and the C-terminal NTPase/helicase domain in solution. These data demonstrate that the hordeivirus TGBp1 has three RNA-binding domains and that interaction between these structural units can provide a basis for remodelling of viral RNP complexes at different steps of cell-to-cell and long-distance transport of virus infection. INTRODUCTIONTransport of plant viruses from cell to cell occurs through plasmodesmata and requires virus-encoded movement proteins (Boevink & Oparka, 2005;Lucas, 2006;Epel, 2009). In the genus Hordeivirus, viral movement proteins are represented by three proteins encoded by a 'triple gene block' (TGB) and referred to as TGBp1, TGBp2 and TGBp3 (Solovyev et al., 1996). The TGB is a conserved module of overlapping genes found in a number of virus groups (Morozov & Solovyev, 2003). Hordeivirus TGBp1 binds viral genomic RNA forming a cell-to-cell transportcompetent complex (Brakke et al., 1988;Kalinina et al., 2001;Lim et al., 2008;Jackson et al., 2009). TGBp2 and TGBp3 are small membrane proteins necessary for intracellular transport of complexes containing TGBp1 and viral RNA to plasmodesmata (Morozov & Solovyev, 2003;Zamyatnin et al., 2004; Haupt et al., 2005;Jackson et al., 2009 Lim et al., 2008;Jackson et al., 2009). Such TGBp1-RNA complexes are considered to be a form of viral genome capable of cell-to-cell and long-distance transport in plants (Morozov & Solovyev, 2003;Lim et al., 2008). In potex-like TGBs, the whole TGBp1 sequence is represented by the NTPase/helicase domain (HELD) with seven conserved motifs of the superfamily 1 NTPases/helicases (Gorbalenya et al., 1989), whereas the hordei-like TGBp1 has an additional N-terminal 'extension region' (Morozov & Solovyev, ...

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Section: Discussionsupporting

confidence: 62%

Domain organization of the N-terminal portion of hordeivirus movement protein TGBp1

Makarov

Rybakova

Ефимов

et al. 2009

Journal of General Virology

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“…Potexviruses are mechanically transmitted (Adams et al, 2004), and maximizing the production of progeny virions might be the main "objective" once cell-tocell movement has been accomplished. TGB1 functions as a MP but also as a translational activator that destabilizes virus particles by binding CP subunits at their 5# end (Atabekov et al, 2000;Kiselyova et al, 2003;Rodionova et al, 2003;Karpova et al, 2006). This destabilization would be problematic for mechanical virion transmission.…”

Section: The X-body Is Not Required For Virus Accumulation and Encapsmentioning

confidence: 99%

The TGB1 Movement Protein ofPotato virus XReorganizes Actin and Endomembranes into the X-Body, a Viral Replication Factory

et al. 2012

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Potato virus X (PVX) requires three virally encoded proteins, the triple gene block (TGB), for movement between cells. TGB1 is a multifunctional protein that suppresses host gene silencing and moves from cell to cell through plasmodesmata, while TGB2 and TGB3 are membrane-spanning proteins associated with endoplasmic reticulum-derived granular vesicles. Here, we show that TGB1 organizes the PVX “X-body,” a virally induced inclusion structure, by remodeling host actin and endomembranes (endoplasmic reticulum and Golgi). Within the X-body, TGB1 forms helically arranged aggregates surrounded by a reservoir of the recruited host endomembranes. The TGB2/3 proteins reside in granular vesicles within this reservoir, in the same region as nonencapsidated viral RNA, while encapsidated virions accumulate at the outer (cytoplasmic) face of the X-body, which comprises a highly organized virus “factory.” TGB1 is both necessary and sufficient to remodel host actin and endomembranes and to recruit TGB2/3 to the X-body, thus emerging as the central orchestrator of the X-body. Our results indicate that the actin/endomembrane-reorganizing properties of TGB1 function to compartmentalize the viral gene products of PVX infection.

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“…VPg has been implicated in potyvirus transport (42,43). Another possible example is provided by the potexviral movement protein TGBp1, which attaches to virions and mediates their destabilization and disassembly in a 5Ј to 3Ј direction (44,45). Given that closteroviruses, potexviruses, and potyviruses belong to distinct evolutionary lineages of positive-strand RNA viruses (46), it seems conceivable that directional intercellular transport could be a general tendency among viruses sharing filamentous virus particle morphology.…”

Section: Discussionmentioning

confidence: 99%

Complex molecular architecture of beet yellows virus particles

Peremyslov

Андреев

Prokhnevsky

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Closteroviruses possess exceptionally long filamentous virus particles that mediate protection and active transport of the genomic RNA within infected plants. These virions are composed of a long ''body'' and short ''tail'' whose principal components are the major and minor capsid proteins, respectively. Here we use biochemical, genetic, and ultrastructural analyses to dissect the molecular composition and architecture of particles of beet yellows virus, a closterovirus. We demonstrate that the virion tails encapsidate the 5-terminal, Ϸ650-nt-long, part of the viral RNA. In addition to the minor capsid protein, the viral Hsp70-homolog, 64-kDa protein, and 20-kDa protein are also incorporated into the virion tail. Atomic force microscopy of virions revealed that the tail possesses a striking, segmented morphology with the tip segment probably being built of 20-kDa protein.The unexpectedly complex structure of closterovirus virions has important mechanistic and functional implications that may also apply to other virus families.atomic force microscopy ͉ closterovirus ͉ RNA encapsidation ͉ virion structure ͉ virus transport

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AFM Study of Potato Virus X Disassembly Induced by Movement Protein

Cited by 61 publications

References 13 publications

Domain organization of the N-terminal portion of hordeivirus movement protein TGBp1

Domain organization of the N-terminal portion of hordeivirus movement protein TGBp1

The TGB1 Movement Protein ofPotato virus XReorganizes Actin and Endomembranes into the X-Body, a Viral Replication Factory

Complex molecular architecture of beet yellows virus particles

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