Interaction of the Trans-Frame Potyvirus Protein P3N-PIPO with Host Protein PCaP1 Facilitates Potyvirus Movement

Vijayapalani, Paramasivan; Maeshima, Masayoshi; Nagasaki-Takekuchi, Nahoko; Miller, W. Allen

doi:10.1371/journal.ppat.1002639

Cited by 173 publications

(199 citation statements)

References 49 publications

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“…Since the PIPO coding sequence was first described in potyviruses, the new gene product P3N-PIPO has attracted much interest, leading to the identification of several important associated functions (8)(9)(10)(11)(12). However, the mechanism by which P3N-PIPO is produced remained unclear until recently, when we and another team independently found evidence that PIPO is expressed by a polymerase slippage mechanism (13,14).…”

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confidence: 99%

The P1N-PISPO trans -Frame Gene of Sweet Potato Feathery Mottle Potyvirus Is Produced during Virus Infection and Functions as an RNA Silencing Suppressor

Mingot

Vallí

Rodamilans

et al. 2016

J Virol

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The positive-sense RNA genome of Sweet potato feathery mottle virus (SPFMV) (genus Potyvirus, family Potyviridae) contains a large open reading frame (ORF) of 3,494 codons translatable as a polyprotein and two embedded shorter ORFs in the ؊1 frame: PISPO, of 230 codons, and PIPO, of 66 codons, located in the P1 and P3 regions, respectively. PISPO is specific to some sweet potato-infecting potyviruses, while PIPO is present in all potyvirids. In SPFMV these two extra ORFs are preceded by conserved G 2 A 6 motifs. We have shown recently that a polymerase slippage mechanism at these sites could produce transcripts bringing these ORFs in frame with the upstream polyprotein, thus leading to P1N-PISPO and P3N-PIPO products (B. Rodamilans, A. IMPORTANCEGene products of potyviruses include P1, HCPro, P3, 6K1, CI, 6K2, VPg/NIaPro, NIb, and CP, all derived from the proteolytic processing of a large polyprotein, and an additional P3N-PIPO product, with the PIPO segment encoded in a different frame within the P3 cistron. In sweet potato feathery mottle virus (SPFMV), another out-of-frame element (PISPO) was predicted within the P1 region. We have shown recently that a polymerase slippage mechanism can generate the transcript variants with extra nucleotides that could be translated into P1N-PISPO and P3N-PIPO. Now, we demonstrate by mass spectrometry analysis that P1N-PISPO is indeed produced in SPFMV-infected plants, in addition to P1. Interestingly, while in other potyviruses the suppressor of RNA silencing is HCPro, we show here that P1N-PISPO exhibited this activity in SPFMV, revealing how the complexity of the gene content could contribute to supply this essential function in members of the Potyviridae family. P otyviruses (family Potyviridae) are important viral pathogens with positive-sense, single-stranded RNA genomes that are able to infect a wide range of plant species. The genomic RNA of potyviruses, around 10 kb in size with a viral protein (VPg) at its 5= end and polyadenylated at the 3= end, contains a large open reading frame (ORF) that encodes a polyprotein comprising the following gene products from the N to the C terminus: P1, HCPro, P3, 6K1, CI, 6K2, VPg/NIaPro, NIb, and CP (1, 2). Despite the abundant sequence information available on potyviruses, it was not until 2008 that the presence of a well-conserved second short ORF of around 60 codons, termed PIPO (Pretty Interesting Potyviral ORF) by its discoverers, was predicted as an overlapping product within the P3 region in all members of the family. Thus, this ORF yields a fusion product with the upstream portion of P3 after frameshift (P3N-PIPO), as found in plants infected with turnip mosaic virus (TuMV) (3). More recently, another short ORF termed PISPO (Pretty Interesting Sweet potato Potyviral ORF) was predicted by bioinformatics analysis within the P1-coding sequence of a few members of the Potyvirus genus, all related to sweet potato feathery mottle virus (SPFMV), including sweet po-

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confidence: 99%

The P1N-PISPO trans -Frame Gene of Sweet Potato Feathery Mottle Potyvirus Is Produced during Virus Infection and Functions as an RNA Silencing Suppressor

Mingot

Vallí

Rodamilans

et al. 2016

J Virol

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“…A small open reading frame (ORF) called PIPO (for pretty interesting Potyviridae ORF) was found to be embedded in the P3 cistron; this ORF can form a functional protein, P3N-PIPO, comprising the N-terminal amino acids of P3 followed by the amino acids encoded by PIPO, which are added presumably through a ϩ2 (or Ϫ1) ribosomal frameshift or transcriptional slippage (39,40). Thus, P3N-PIPO has the same N-terminal part (P3N) as P3 and P3N-PIPO of Turnip mosaic virus (TuMV) appears to interact with CI in the plasmodesmata of Nicotiana benthamiana and facilitate movement of viral RNA to neighboring cells (40)(41)(42).…”

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confidence: 99%

“…Thus, P3N-PIPO has the same N-terminal part (P3N) as P3 and P3N-PIPO of Turnip mosaic virus (TuMV) appears to interact with CI in the plasmodesmata of Nicotiana benthamiana and facilitate movement of viral RNA to neighboring cells (40)(41)(42). These studies indicate that both P3 and P3N-PIPO are essential proteins for potyvirus infection and thus have the potential to be the virulence determinant in viruses that can overcome resistance in cyv1 and sbm-2 pea.…”

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confidence: 99%

Quantitative and Qualitative Involvement of P3N-PIPO in Overcoming Recessive Resistance against Clover Yellow Vein Virus in Pea Carrying the cyv1 Gene

Choi

Hagiwara‐Komoda

Nakahara

et al. 2013

J Virol

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In pea carrying cyv1, a recessive gene for resistance to Clover yellow vein virus (ClYVV), ClYVV isolate Cl-no30 was restricted to the initially infected cells, whereas isolate 90-1 Br2 overcame this resistance. We mapped the region responsible for breaking of cyv1-mediated resistance by examining infection of cyv1 pea with chimeric viruses constructed from parts of Cl-no30 and 90-1 Br2. The breaking of resistance was attributed to the P3 cistron, which is known to produce two proteins: P3, from the main open reading frame (ORF), and P3N-PIPO, which has the N-terminal part of P3 fused to amino acids encoded by a small open reading frame (ORF) called PIPO in the ؉2 reading frame. We introduced point mutations that were synonymous with respect to the P3 protein but nonsynonymous with respect to the P3N-PIPO protein, and vice versa, into the chimeric viruses. Infection of plants with these mutant viruses revealed that both P3 and P3N-PIPO were involved in overcoming cyv1-mediated resistance. Moreover, P3N-PIPO quantitatively affected the virulence of Cl-no30 in cyv1 pea. Additional expression in trans of the P3N-PIPO derived from Cl-no30, using White clover mosaic virus as a vector, enabled Cl-no30 to move to systemic leaves in cyv1 pea. Susceptible pea plants infected with chimeric ClYVV possessing the P3 cistron of 90-1 Br2, and which were therefore virulent toward cyv1 pea, accumulated more P3N-PIPO than did those infected with Cl-no30, suggesting that the higher level of P3N-PIPO in infected cells contributed to the breaking of resistance by 90-1 Br2. This is the first report showing that P3N-PIPO is a virulence determinant in plants resistant to a potyvirus.

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“…Moreover, a sub-population of particles isolated from plants infected with Potato virus A has been shown to contain the viral CI (cylindrical inclusion) protein localized to one end of the virion (GabrenaiteVerkhovskaya et al, 2008), presumably due to the reported ability of CI to interact with HC-Pro (Revers & García, 2015). The CI protein is targeted to plasmodesmata-associated sites by the recently discovered CI-interacting potyvirus protein P3N-PIPO, which is essential for viral transport and is capable of directed intracellular trafficking to plasmodesmata and translocation through plasmodesmata to neighbouring cells (Chung et al, 2008;Vijayapalani et al, 2012).…”

Section: Role Of Virions In Cell-to-cell Transport Of Filamentous Virmentioning

confidence: 99%

Helical capsids of plant viruses: architecture with structural lability

Solovyev

Makarov

2016

Journal of General Virology

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Capsids of numerous filamentous and rod-shaped plant viruses possess helical symmetry. In positive-stranded RNA viruses, helical capsids are typically composed of many identical subunits of the viral capsid protein (CP), encapsidating a molecule of viral genomic RNA. Current progress in structural studies of helical plant viruses has revealed differences between filamentous and rod-shaped viruses, both in structural folds of their CPs and in the interactions of CP molecules in their capsids. Many filamentous and rod-shaped viruses have functionally similar lateral inter-subunit contacts on the outer virion surface. Additionally, the extreme Nterminal CP region in filamentous viruses is intrinsically disordered. Taken together, the available data establish a link between the structural features of molecular interactions of CP molecules and the physical properties of helical virions ranging from rigidity to flexibility. Overall, the structure of helical plant viruses is significantly more labile than previously thought, often allowing structural transitions, remodelling and the existence of alternative structural forms of virions. These properties of virions are believed to be functionally significant at certain stages of the viral life cycle, such as during translational activation and cell-to-cell transport. In this review, we discuss structural and functional features of filamentous and rod-shaped virions, highlight their shared features and differences, and lay emphasis on the relationships between the molecular structure of viral capsids and their properties including virion shape, lability and capability of structural remodelling.

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Interaction of the Trans-Frame Potyvirus Protein P3N-PIPO with Host Protein PCaP1 Facilitates Potyvirus Movement

Cited by 173 publications

References 49 publications

The P1N-PISPO trans -Frame Gene of Sweet Potato Feathery Mottle Potyvirus Is Produced during Virus Infection and Functions as an RNA Silencing Suppressor

The P1N-PISPO trans -Frame Gene of Sweet Potato Feathery Mottle Potyvirus Is Produced during Virus Infection and Functions as an RNA Silencing Suppressor

Quantitative and Qualitative Involvement of P3N-PIPO in Overcoming Recessive Resistance against Clover Yellow Vein Virus in Pea Carrying the cyv1 Gene

Helical capsids of plant viruses: architecture with structural lability

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