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Open AccessArticle

Potyvirus HcPro Suppressor of RNA Silencing Induces PVY Superinfection Exclusion in a Strain-Specific Manner

by Vincent N. Fondong and Prakash M. Niraula

Int. J. Mol. Sci. 2025, 26(23), 11644; https://doi.org/10.3390/ijms262311644 - 1 Dec 2025

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The potyvirus helper component proteinase (HcPro) is a multifunctional protein, with one of its most documented functions being host antiviral RNA silencing suppression. This study shows that the HcPro of potato virus Y (PVY), an important member of the potyvirus group, prevents the replication of a related competing secondary virus. This phenomenon, referred to as superinfection exclusion (SIE), is common in bacterial, human, and plant virus infections. We also report that HcPro’s induction of SIE is strain-specific and that this specificity is provided by the first four amino acid residues of the protein. Consistent with the mechanism of SIE, the study found that HcPro does not exclude a resident virus. Additionally, HcPro’s induction of SIE was observed to function independently of its ability to suppress antiviral RNA silencing. HcPro’s induction of SIE is relevant given the prevalence of multiple PVY strains that routinely co-infect the same cell and that may lead to recombination and emergence of new and more virulent strains. Furthermore, cross-protection or systemic acquired resistance (SAR) that is employed in plant virus disease management occurs when SIE moves from the cellular level and spreads systemically, emphasizing the importance of studying SIE. Full article

(This article belongs to the Special Issue Viral Infections and Viral Pathogenesis)

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12 pages, 855 KB

Open AccessArticle

A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum

by Benoît Moury, Thierry Michon, Vincent Simon and Alain Palloix

Viruses 2023, 15(5), 1081; https://doi.org/10.3390/v15051081 - 28 Apr 2023

Cited by 1 | Viewed by 1991

Abstract

The dominant Pvr4 gene in pepper (Capsicum annuum) confers resistance to members of six potyvirus species, all of which belong to the Potato virus Y (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cistron (i.e., RNA-dependent RNA polymerase). Here, we describe a new source of potyvirus resistance in the Guatemalan accession C. annuum cv. PM949. PM949 is resistant to members of at least three potyvirus species, a subset of those controlled by Pvr4. The F₁ progeny between PM949 and the susceptible cultivar Yolo Wonder was susceptible to PVY, indicating that the resistance is recessive. The segregation ratio between resistant and susceptible plants observed in the F₂ progeny matched preferably with resistance being determined by two unlinked recessive genes independently conferring resistance to PVY. Inoculations by grafting resulted in the selection of PVY mutants breaking PM949 resistance and, less efficiently, Pvr4–mediated resistance. The codon substitution E₄₇₂K in the NIb cistron of PVY, which was shown previously to be sufficient to break Pvr4 resistance, was also sufficient to break PM949 resistance, a rare example of cross-pathogenicity effect. In contrast, the other selected NIb mutants showed specific infectivity in PM949 or Pvr4 plants. Comparison of Pvr4 and PM949 resistance, which share the same target in PVY, provides interesting insights into the determinants of resistance durability. Full article

(This article belongs to the Special Issue Plant Virus Resistance)

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16 pages, 3506 KB

Open AccessArticle

Adaptation of a Potyvirus Chimera Increases Its Virulence in a Compatible Host through Changes in HCPro

by Hao Sun, Francisco del Toro, Mongia Makki, Francisco Tenllado and Tomas Canto

Plants 2022, 11(17), 2262; https://doi.org/10.3390/plants11172262 - 30 Aug 2022

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Abstract

A viral chimera in which the P1-HCPro bi-cistron of a plum pox virus construct (PPV-GFP) was replaced by that of potato virus Y (PVY) spread slowly systemically in Nicotiana benthamiana plants and accumulated to levels that were 5−10% those of parental PPV-GFP. We tested whether consecutive mechanical passages could increase its virulence, and found that after several passages, chimera titers rose and symptoms increased. We sequenced over half the genome of passaged chimera lineages infecting two plants. The regions sequenced were 5′NCR-P1-HCPro-P3; Vpg/NIa; GFP-CP, because of being potential sites for mutations/deletions leading to adaptation. We found few substitutions, all non-synonymous: two in one chimera (nt 2053 HCPro, and 5733 Vpg/NIa), and three in the other (2359 HCPro, 5729 Vpg/NIa, 9466 CP). HCPro substitutions 2053 AUU(Ile)→ACU(Thr), and 2359 CUG(Leu)→CGG(Arg) occurred at positions where single nucleotide polymorphisms were observed in NGS libraries of sRNA reads from agroinfiltrated plants (generation 1). Remarkably, position 2053 was the only one in the sequenced protein-encoding genome in which polymorphisms were common to the four libraries, suggesting that selective pressure existed to alter that specific nucleotide, previous to any passage. Mutations 5729 and 5733 in the Vpg by contrast did not correlate with polymorphisms in generation 1 libraries. Reverse genetics showed that substitution 2053 alone increased several-fold viral local accumulation, speed of systemic spread, and systemic titers. Full article

(This article belongs to the Special Issue Advances in Plant Viral Diseases)

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16 pages, 2406 KB

Open AccessFeature PaperArticle

Differences in Virulence among PVY Isolates of Different Geographical Origins When Infecting an Experimental Host under Two Growing Environments Are Not Determined by HCPro

by Mongia Makki, Francisco Javier del Toro, Khouloud Necira, Francisco Tenllado, Fattouma Djilani-Khouadja and Tomás Canto

Plants 2021, 10(6), 1086; https://doi.org/10.3390/plants10061086 - 28 May 2021

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Abstract

The contribution of the HCPro factors expressed by several PVY isolates of different geographical origins (one from Scotland, one from Spain, and several from Tunisia) to differences in their virulence in Nicotiana benthamiana plants was investigated under two growing conditions: standard (st; 26 °C and current ambient levels of CO₂), and climate change-associated (cc; 31 °C and elevated levels of CO₂). In all cases, relative infection symptoms and viral titers were determined. The viral HCPro cistrons were also sequenced and amino-acid features of the encoded proteins were established, as well as phylogenetic distances. Additionally, the abilities of the HCPros of several isolates to suppress silencing were assessed under either growing condition. Overall, viral titers and infection symptoms decreased under cc vs. st conditions. However, within each growing condition, relative titers and symptoms were found to be isolate-specific, with titers and symptom severities not always correlating. Crucially, isolates expressing identical HCPros displayed different symptoms. In addition, all HCPro variants tested displayed comparable silencing suppression strengths. Therefore, HCPro alone could not be the main determinant of the relative differences in pathogenicity observed among the PVY isolates tested in this host, under the environments considered. Full article

(This article belongs to the Section Plant Protection and Biotic Interactions)

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24 pages, 20656 KB

Open AccessArticle

A Novel Interaction Network Used by Potyviruses in Virus–Host Interactions at the Protein Level

by Marjo Ala-Poikela, Minna-Liisa Rajamäki and Jari P.T. Valkonen

Viruses 2019, 11(12), 1158; https://doi.org/10.3390/v11121158 - 14 Dec 2019

Cited by 25 | Viewed by 6481

Abstract

Host proteins that are central to infection of potyviruses (genus Potyvirus; family Potyviridae) include the eukaryotic translation initiation factors eIF4E and eIF(iso)4E. The potyviral genome-linked protein (VPg) and the helper component proteinase (HCpro) interact with each other and with eIF4E and eIF(iso)4E and proteins are involved in the same functions during viral infection. VPg interacts with eIF4E/eIF(iso)4E via the 7-methylguanosine cap-binding region, whereas HCpro interacts with eIF4E/eIF(iso)4E via the 4E-binding motif YXXXXLΦ, similar to the motif in eIF4G. In this study, HCpro and VPg were found to interact in the nucleus, nucleolus, and cytoplasm in cells infected with the potyvirus potato virus A (PVA). In the cytoplasm, interactions between HCpro and VPg occurred in punctate bodies not associated with viral replication vesicles. In addition to HCpro, the 4E-binding motif was recognized in VPg of PVA. Mutations in the 4E-binding motif of VPg from PVA weakened interactions with eIF4E and heavily reduced PVA virulence. Furthermore, mutations in the 4G-binding domain of eIF4E reduced interactions with VPg and abolished interactions with HCpro. Thus, HCpro and VPg can both interact with eIF4E using the 4E-binding motif. Our results suggest a novel interaction network used by potyviruses to interact with host plants via translation initiation factors. Full article

(This article belongs to the Special Issue The Complexity of the Potyviral Interaction Network)

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