The role of plasmodesma-located proteins in tubule-guided virus transport is limited to the plasmodesmata

Hollander, P. W. den; Kieper, Sebastian N.; Borst, J.W.; Lent, J.W.M. van

doi:10.1007/s00705-016-2936-2

Cited by 16 publications

(12 citation statements)

References 29 publications

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“…Consistent with the tubule assembly from MP, the monomers of the tubule-forming MPs of caulimoand nepoviruses showed MP-MP interactions in vivo (27). Moreover, these proteins were shown to interact with members of the PDLP family at PD (27,28). Amari et al (27) showed that both the MP of grapevine fanleaf virus (GFLV) and the MP of cauliflower mosaic virus (CaMV) interact with PDLPs at PDs and that the systemic movement of both viruses was inhibited in pdlp1 pdlp2 pdlp3 triple-knockout Arabidopsis thaliana mutants (27).…”

Section: Resultsmentioning

confidence: 64%

“…The interaction with the PDLP family of proteins might be a common feature of the tubule-forming viruses. Consistently, the tubule-forming MP of cowpea mosaic virus (CPMV) was also shown to interact with PDLP1 in vivo (28). To determine whether MP CPsV has the capacity to interact with PDLP1, we used fluorescence lifetime imaging microscopy (FLIM) to measure the degree of fluorescence resonance emission transfer (FRET) between the GFP and monomeric red fluorescent protein (RFP) moieties of MP CPsV :GFP and PDLP1:RFP expressed in N. benthamiana epidermal cells.…”

Section: Resultsmentioning

confidence: 99%

“…Unlike the MP of TMV and presumably the MPs of other viruses moving by the non-tubule-mediated mechanism, the MPs of tubule-forming viruses interact with members of the PD-located protein (PDLP) family, and this interaction is required for tubule assembly and the spread of infection (27,28). PDLPs require the ER-Golgi pathway for their targeting to PD (27,29), which may explain the observed sensitivity of tubule formation and tubule-mediated virus movement to secretory pathway inhibitors (27,30,31).…”

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confidence: 99%

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Citrus Psorosis Virus Movement Protein Contains an Aspartic Protease Required for Autocleavage and the Formation of Tubule-Like Structures at Plasmodesmata

Luna

Peña

Borniego

et al. 2018

J Virol

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Plant virus cell-to-cell movement is an essential step in viral infections. This process is facilitated by specific virus-encoded movement proteins (MPs), which manipulate the cell wall channels between neighboring cells known as plasmodesmata (PD). Citrus psorosis virus (CPsV) infection in sweet orange involves the formation of tubule-like structures within PD, suggesting that CPsV belongs to "tubule-forming" viruses that encode MPs able to assemble a hollow tubule extending between cells to allow virus movement. Consistent with this hypothesis, we show that the MP of CPsV (MP) indeed forms tubule-like structures at PD upon transient expression in leaves. Tubule formation by MP depends on its cleavage capacity, mediated by a specific aspartic protease motif present in its primary sequence. A single amino acid mutation in this motif abolishes MP cleavage, alters the subcellular localization of the protein, and negatively affects its activity in facilitating virus movement. The amino-terminal 34-kDa cleavage product (34K), but not the 20-kDa fragment (20K), supports virus movement. Moreover, similar to tubule-forming MPs of other viruses, MP (and also the 34K cleavage product) can homooligomerize, interact with PD-located protein 1 (PDLP1), and assemble tubule-like structures at PD by a mechanism dependent on the secretory pathway. 20K retains the protease activity and is able to cleave a cleavage-deficient MP in Altogether, these results demonstrate that CPsV movement depends on the autolytic cleavage of MP by an aspartic protease activity, which removes the 20K protease and thereby releases the 34K protein for PDLP1-dependent tubule formation at PD. Infection by citrus psorosis virus (CPsV) involves a self-cleaving aspartic protease activity within the viral movement protein (MP), which results in the production of two peptides, termed 34K and 20K, that carry the MP and viral protease activities, respectively. The underlying protease motif within the MP is also found in the MPs of other members of the family, suggesting that protease-mediated protein processing represents a conserved mechanism of protein expression in this virus family. The results also demonstrate that CPsV and potentially other ophioviruses move by a tubule-guided mechanism. Although several viruses from different genera were shown to use this mechanism for cell-to-cell movement, our results also demonstrate that this mechanism is controlled by posttranslational protein cleavage. Moreover, given that tubule formation and virus movement could be inhibited by a mutation in the protease motif, targeting the protease activity for inactivation could represent an important approach for ophiovirus control.

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Section: Resultsmentioning

confidence: 64%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Citrus Psorosis Virus Movement Protein Contains an Aspartic Protease Required for Autocleavage and the Formation of Tubule-Like Structures at Plasmodesmata

Luna

Peña

Borniego

et al. 2018

J Virol

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“…However, there is a special protein class of ‘30-kDa’-like MPs [30] , which use an alternative mechanism for cell-to-cell transport. This mechanism includes the displacement of the Pd internal structures including the desmotubule by a tubular structure formed by viral MP and the transfer of whole virions inside the tubule from infected cells to neighboring cells [9] , [12] , [18] , [31] . Virions can pass Pd inside MP-formed tubule in some positive strand RNA viruses, namely, comoviruses and nepoviruses (family Secoviridae ) [31] , [32] , and pararetroviruses [18] , [33] – [37] .…”

Section: Introductionmentioning

confidence: 99%

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

Morozov

Solovyev

2020

AIMS Microbiology

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Most plant viruses code for movement proteins (MPs) targeting plasmodesmata to enable cell-to-cell and systemic spread in infected plants. Small membrane-embedded MPs have been first identified in two viral transport gene modules, triple gene block (TGB) coding for an RNA-binding helicase TGB1 and two small hydrophobic proteins TGB2 and TGB3 and double gene block (DGB) encoding two small polypeptides representing an RNA-binding protein and a membrane protein. These findings indicated that movement gene modules composed of two or more cistrons may encode the nucleic acid-binding protein and at least one membrane-bound movement protein. The same rule was revealed for small DNA-containing plant viruses, namely, viruses belonging to genus Mastrevirus (family Geminiviridae ) and the family Nanoviridae . In multi-component transport modules the nucleic acid-binding MP can be viral capsid protein(s), as in RNA-containing viruses of the families Closteroviridae and Potyviridae . However, membrane proteins are always found among MPs of these multicomponent viral transport systems. Moreover, it was found that small membrane MPs encoded by many viruses can be involved in coupling viral replication and cell-to-cell movement. Currently, the studies of evolutionary origin and functioning of small membrane MPs is regarded as an important pre-requisite for understanding of the evolution of the existing plant virus transport systems. This paper represents the first comprehensive review which describes the whole diversity of small membrane MPs and presents the current views on their role in plant virus movement.

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“…Virus particles in a linear formation are often observed inside these tubular structures. These VTs may be able to grow in cell walls containing plasmodesmata and outward into neighboring cells to deliver viruses . This group of viruses includes alfalfa mosaic virus (AMV, genus Alfamovirus ), cowpea mosaic virus (CPMV, genus Comovirus ), brome mosaic virus (BMV, genus Bromovirus ), cucumber mosaic virus (CMV, genus Cucumovirus ), and prunus necrotic ringspot virus (PNRSV, genus Ilarvirus ) .…”

Section: Introductionmentioning

confidence: 99%

Morphological Characterization of the Self‐Assembly of Virus Movement Proteins into Nanotubes in the Absence of Virus Particles

et al. 2017

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One infection mechanism of plant viruses is the generation of nanotubes by viral movement proteins, allowing cell‐to‐cell virus particle transport. Previously, it was assumed that viral nanotubes extend directly from the host‐cell plasma membrane. In virus‐infected plants, these nanotubes reach an extraordinary diameter:length ratio (≈100 nm:µm or mm range). Here, viral nanotubes are produced in a transient protoplast system; the coding sequence for alfalfa mosaic virus movement protein is translationally fused to green fluorescent protein. The maximum extension of viral nanotubes into the culture medium is achieved 24–48 h posttransfection, with lengths in the micro‐ and millimeter ranges. Scanning electron microscopy and transmission electron microscopy show that strong inhomogeneous viral nanotubes are formed compared to particle‐filled systems. The nanotubes have similar length, but fluctuating wall thickness and diameter and are susceptible to entanglement and recombination. Indirect methods demonstrate that movement proteins assemble independently at the top of the nanotube. These viral nanotubes grow distinctly from previously known natural particle‐filled systems and are a unique biological tubular nanomaterial that has the potential for micro‐ or nanoapplications as a mechanically stable structural component.

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The role of plasmodesma-located proteins in tubule-guided virus transport is limited to the plasmodesmata

Cited by 16 publications

References 29 publications

Citrus Psorosis Virus Movement Protein Contains an Aspartic Protease Required for Autocleavage and the Formation of Tubule-Like Structures at Plasmodesmata

Citrus Psorosis Virus Movement Protein Contains an Aspartic Protease Required for Autocleavage and the Formation of Tubule-Like Structures at Plasmodesmata

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

Morphological Characterization of the Self‐Assembly of Virus Movement Proteins into Nanotubes in the Absence of Virus Particles

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