Tritimovirus P1 functions as a suppressor of RNA silencing and an enhancer of disease symptoms

Young, Brock A.; Stenger, Drake C.; Qu, Feng; Morris, T. Jack; Satyanarayana, T.; French, Ron

doi:10.1016/j.virusres.2011.12.019

Cited by 63 publications

(42 citation statements)

References 53 publications

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“…Additionally, accumulation of abundant vsiRNAs in doubly infected wheat cultivars shows that the presence of two silencing suppressors did not inhibit the biogenesis of virus-derived small RNAs. Our previous work demonstrated that silencing suppressor proteins of WSMV and TriMV repressed host RNA silencing by inhibiting production of vsiRNAs [55], [56]. Taken together, these data suggest that synergism results from events that occur downstream of vsiRNA biogenesis; hence, synergistic interaction and RNA silencing are likely unrelated.…”

Section: Discussionmentioning

confidence: 79%

“…However, in Mace, double infections induced moderate disease synergism at 20 to 26°C but not at 19°C. The P1 proteins of WSMV and TriMV have been reported to be involved in the suppression of local and systemic RNA silencing in N. benthamiana 16c plants [55], [56]. However, the response of wheat defense mechanisms against single and double infections in susceptible and resistant wheat cultivars with WSMV and TriMV has not been examined, and it is not known how viral infection(s) trigger cascades of host defense mechanisms that cause production of vsiRNAs, an important component of host RNA silencing.…”

Section: Introductionmentioning

confidence: 99%

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Dynamics of Small RNA Profiles of Virus and Host Origin in Wheat Cultivars Synergistically Infected by Wheat Streak Mosaic Virus and Triticum Mosaic Virus: Virus Infection Caused a Drastic Shift in the Endogenous Small RNA Profile

et al. 2014

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Co-infection of wheat (Triticum aestivum L.) by Wheat streak mosaic virus (WSMV, a Tritimovirus) and Triticum mosaic virus (TriMV, a Poacevirus) of the family Potyviridae causes synergistic interaction. In this study, the effects of the synergistic interaction between WSMV and TriMV on endogenous and virus-derived small interfering RNAs (vsiRNAs) were examined in susceptible (‘Arapahoe’) and temperature-sensitive resistant (‘Mace’) wheat cultivars at 18°C and 27°C. Single and double infections in wheat caused a shift in the profile of endogenous small RNAs from 24 nt being the most predominant in healthy plants to 21 nt in infected wheat. Massive amounts of 21 and 22 nt vsiRNAs accumulated in singly and doubly infected Arapahoe at both temperatures and in Mace at 27°C but not 18°C. The plus- and minus-sense vsiRNAs were distributed throughout the genomic RNAs in Arapahoe at both temperature regimens and in Mace at 27°C, although some regions served as hot-spots, spawning an excessive number of vsiRNAs. The vsiRNA peaks were conserved among cultivars, suggesting that the Dicer-like enzymes in susceptible and resistant cultivars similarly accessed the genomic RNAs of WSMV or TriMV. Accumulation of large amounts of vsiRNAs in doubly infected plants suggests that the silencing suppressor proteins encoded by TriMV and WSMV do not prevent the formation of vsiRNAs; thus, the synergistic effect observed is independent from RNA-silencing mediated vsiRNA biogenesis. The high-resolution map of endogenous and vsiRNAs from WSMV- and/or TriMV-infected wheat cultivars may form a foundation for understanding the virus-host interactions, the effect of synergistic interactions on host defense, and virus resistance mechanisms in wheat.

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Section: Discussionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Dynamics of Small RNA Profiles of Virus and Host Origin in Wheat Cultivars Synergistically Infected by Wheat Streak Mosaic Virus and Triticum Mosaic Virus: Virus Infection Caused a Drastic Shift in the Endogenous Small RNA Profile

et al. 2014

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“…Interestingly, for all the members of the Potyvirus genus tested so far, the essential RNA silencing suppression activity was found associated with HCPro, which was the first characterized RSS (54,55). In other members of the Potyviridae family, however, the RNA silencing suppression function is often shifted to P1 products, as has been observed in ipomoviruses (18,33,56), tritimoviruses (57), and poaceviruses (58). These RSSs belong to a distinct group of P1 proteins that appears to be evolutionarily separated from typical P1 proteins of members of the genus Potyvirus (7,59).…”

Section: Discussionmentioning

confidence: 89%

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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“…In contrast to the multifunctional potyviral HC-Pro (23), WSMV HC-Pro is dispensable for systemic infection (41). P1 of WSMV, and not HC-Pro as in potyviruses, was identified as the suppressor of RNA silencing (42).…”

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confidence: 97%

Wheat streak mosaic virus Infects Systemically despite Extensive Coat Protein Deletions: Identification of Virion Assembly and Cell-to-Cell Movement Determinants

Satyanarayana

Kovacs

French

2014

J Virol

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b Viral coat proteins function in virion assembly and virus biology in a tightly coordinated manner with a role for virtually every amino acid. In this study, we demonstrated that the coat protein (CP) of Wheat streak mosaic virus (WSMV; genus Tritimovirus, family Potyviridae) is unusually tolerant of extensive deletions, with continued virion assembly and/or systemic infection found after extensive deletions are made. A series of deletion and point mutations was created in the CP cistron of wild-type and/or green fluorescent protein-tagged WSMV, and the effects of these mutations on cell-to-cell and systemic transport and virion assembly of WSMV were examined. Mutants with overlapping deletions comprising N-terminal amino acids 6 to 27, 36 to 84, 85 to 100, 48 to 100, and 36 to 100 or the C-terminal 14 or 17 amino acids systemically infected wheat with different efficiencies. However, mutation of conserved amino acids in the core domain, which may be involved in a salt bridge, abolished virion assembly and cell-to-cell movement. N-terminal amino acids 6 to 27 and 85 to 100 are required for efficient virion assembly and cell-to-cell movement, while the C-terminal 65 amino acids are dispensable for virion assembly but are required for cell-to-cell movement, suggesting that the C terminus of CP functions as a dedicated cell-to-cell movement determinant. In contrast, amino acids 36 to 84 are expendable, with their deletion causing no obvious effects on systemic infection or virion assembly. In total, 152 amino acids (amino acids 6 to 27 and 36 to 100 and the 65 amino acids at the C-terminal end) of 349 amino acids of CP are dispensable for systemic infection and/or virion assembly, which is rare for multifunctional viral CPs.

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Tritimovirus P1 functions as a suppressor of RNA silencing and an enhancer of disease symptoms

Cited by 63 publications

References 53 publications

Dynamics of Small RNA Profiles of Virus and Host Origin in Wheat Cultivars Synergistically Infected by Wheat Streak Mosaic Virus and Triticum Mosaic Virus: Virus Infection Caused a Drastic Shift in the Endogenous Small RNA Profile

Dynamics of Small RNA Profiles of Virus and Host Origin in Wheat Cultivars Synergistically Infected by Wheat Streak Mosaic Virus and Triticum Mosaic Virus: Virus Infection Caused a Drastic Shift in the Endogenous Small RNA Profile

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

Wheat streak mosaic virus Infects Systemically despite Extensive Coat Protein Deletions: Identification of Virion Assembly and Cell-to-Cell Movement Determinants

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