Dissecting the Molecular Mechanism of the Subcellular Localization and Cell-to-cell Movement of the Sugarcane mosaic virus P3N-PIPO

Cheng, Guangyuan; Meng, Dong; Xu, Qian; Lei, Peng; Yang, Zongtao; Wèi, Tàiyún; Xu, Jianhong

doi:10.1038/s41598-017-10497-6

Cited by 22 publications

(23 citation statements)

References 60 publications

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“…The distribution of P3N-PIPO under the condition of TuMV infection was also analyzed with the same strategy. Consistent with previous studies (16,20), P3N-PIPO-YFP was located mainly on the plasma membrane, which also contained PDs in the cells infected with TuMV-6K2mCh (Fig. 4E).…”

Section: Resultssupporting

confidence: 92%

“…P3N-PIPO functions in cell-to-cell movement by interacting with CI and targeting it to the PD (16). Moreover, a study on Sugarcane mosaic virus (SCMV) showed that P3N-PIPO interacts with both CI and PCaP1 via its C-terminal PIPO domain (20). BiFC assays showed that TuMV CI also interacts with P3N-PIPO via the PIPO domain (Fig.…”

Section: Resultsmentioning

confidence: 95%

“…P3N-PIPO also interacts with several host factors (18,19); however, the roles of these interactions in potyviral intercellular movement still need to be investigated. P3N-PIPO interacts with CI via its C-terminal PIPO domain and directs CI to the PD to form a conical structure for intercellular movement (16,20). CP is also indispensable for movement, since Tobacco etch virus (TEV) mutants containing CPs with a substitution of the highly conserved Ser122 within the core domain or with a 17-amino-acid (aa) deletion at the C-terminal domain and Soybean mosaic virus (SMV) mutants containing CPs with single substitutions of the charged amino acids in the C-proximal region are defective in movement (21,22).…”

mentioning

confidence: 99%

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P3N-PIPO Interacts with P3 via the Shared N-Terminal Domain To Recruit Viral Replication Vesicles for Cell-to-Cell Movement

Chai

Liu

et al. 2020

J Virol

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P3N-PIPO, the only dedicated movement protein (MP) of potyviruses, directs cylindrical inclusion (CI) protein from the cytoplasm to the plasmodesma (PD), where CI forms conical structures for intercellular movement. To better understand potyviral cell-to-cell movement, we further characterized P3N-PIPO using Turnip mosaic virus (TuMV) as a model virus. We found that P3N-PIPO interacts with P3 via the shared P3N domain and that TuMV mutants lacking the P3N domain of either P3N-PIPO or P3 are defective in cell-to-cell movement. Moreover, we found that the PIPO domain of P3N-PIPO is sufficient to direct CI to the PD, whereas the P3N domain is necessary for localization of P3N-PIPO to 6K2-labeled vesicles or aggregates. Finally, we discovered that the interaction between P3 and P3N-PIPO is essential for the recruitment of CI to cytoplasmic 6K2-containing structures and the association of 6K2-containing structures with PD-located CI inclusions. These data suggest that both P3N and PIPO domains are indispensable for potyviral cell-to-cell movement and that the 6K2 vesicles in proximity to PDs resulting from multipartite interactions among 6K2, P3, P3N-PIPO, and CI may also play an essential role in this process. IMPORTANCE Potyviruses include numerous economically important viruses that represent approximately 30% of known plant viruses. However, there is still limited information about the mechanism of potyviral cell-to-cell movement. Here, we show that P3N-PIPO interacts with and recruits CI to the PD via the PIPO domain and interacts with P3 via the shared P3N domain. We further report that the interaction of P3N-PIPO and P3 is associated with 6K2 vesicles and brings the 6K2 vesicles into proximity with PD-located CI structures. These results support the notion that the replication and cell-to-cell movement of potyviruses are processes coupled by anchoring viral replication complexes at the entrance of PDs, which greatly increase our knowledge of the intercellular movement of potyviruses.

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Section: Resultssupporting

confidence: 92%

Section: Resultsmentioning

confidence: 95%

mentioning

confidence: 99%

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P3N-PIPO Interacts with P3 via the Shared N-Terminal Domain To Recruit Viral Replication Vesicles for Cell-to-Cell Movement

Chai

Liu

et al. 2020

J Virol

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“…Considering that TuMV is synergistic with Cucumber mosaic virus (CMV) and promotes the cell‐to‐cell movement of the transport‐deficient isolate CMV‐Y (Takeshita & Takanami, ), we speculate that PD actin filament depolymerisation may contribute to this synergism. The homologues of PCaP1 not only interact with the P3N‐PIPO of TuMV (Vijayapalani et al ., ) but also those of Tobacco vein banding mosaic virus (Geng et al ., ) or Sugarcane mosaic virus (Cheng et al ., ), which implicates a general requirement for PCaP1 in potyviral cell‐to‐cell movement. However, TuMV eventually establishes systemic infection in pcap1 (Vijayapalani et al ., ) or P PCaP1 :PCaP1 N5A ; pcap1 in the present work, indicating that PCaP1 may be involved in the early stage of TuMV infection, or other actin filament‐severing proteins are involved in TuMV infection.…”

Section: Discussionmentioning

confidence: 77%

Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg

et al. 2019

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Group 1 Remorins (REMs) are extensively involved in virus trafficking through plasmodesmata (PD). However, their roles in Potyvirus cell-to-cell movement are not known. The plasma membrane (PM)-associated Ca 2+ binding protein 1 (PCaP1) interacts with the P3N-PIPO of Turnip mosaic virus (TuMV) and is required for TuMV cell-to-cell movement, but the underlying mechanism remains elusive.The mutant plants with overexpression or knockout of REM1.2 were used to investigate its role in TuMV cell-to-cell movement. Arabidopsis thaliana complementary mutants of pcap1 were used to investigate the role of PCaP1 in TuMV cell-to-cell movement. Yeast-two-hybrid, bimolecular fluorescence complementation, co-immunoprecipitation and RT-qPCR assays were employed to investigate the underlying molecular mechanism.The results show that TuMV-P3N-PIPO recruits PCaP1 to PD and the actin filament-severing activity of PCaP1 is required for TuMV intercellular movement. REM1.2 negatively regulates the cell-to-cell movement of TuMV via competition with PCaP1 for binding actin filaments. As a counteractive response, TuMV mediates REM1.2 degradation via both 26S ubiquitin-proteasome and autophagy pathways through the interaction of VPg with REM1.2 to establish systemic infection in Arabidopsis.This work unveils the actin cytoskeleton and PM nanodomain-associated molecular events underlying the cell-to-cell movement of potyviruses.

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“…Further movement of VRC to cell periphery and PD requires a nonconventional pathway bypassing ER-Golgi trafficking and involving VTI11, a pre-vacuolar compartment SNARE protein [84] . P3N-PIPO, which binds to VRC through P3-P3N interactions [72] , is a critical component of VRC vesicles specifically required for the PD targeting, and the PD association of P3N-PIPO depends on the PIPO domain [85] .…”

Section: Potyvirusesmentioning

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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Dissecting the Molecular Mechanism of the Subcellular Localization and Cell-to-cell Movement of the Sugarcane mosaic virus P3N-PIPO

Cited by 22 publications

References 60 publications

P3N-PIPO Interacts with P3 via the Shared N-Terminal Domain To Recruit Viral Replication Vesicles for Cell-to-Cell Movement

P3N-PIPO Interacts with P3 via the Shared N-Terminal Domain To Recruit Viral Replication Vesicles for Cell-to-Cell Movement

Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg

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

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