publication . Article . 2015

A novel sweet potato potyvirus open reading frame (ORF) is expressed via polymerase slippage and suppresses RNA silencing

Untiveros, Milton; Olspert, Allan; Artola, Katrin; Firth, Andrew E.; Kreuze, Jan F.; Valkonen, Jari P. T.;
Open Access English
  • Published: 22 Dec 2015 Journal: volume 17, issue 7, pages 1,111-1,123issn: 1464-6722, eissn: 1364-3703, Copyright policy
  • Publisher: Molecular Plant Pathology
Abstract
The single-stranded, positive-sense RNA genome of viruses in the genus Potyvirus encodes a large polyprotein that is cleaved to yield 10 mature proteins. The first three cleavage products are P1, HCpro and P3. An additional short open reading frame (ORF), called pipo, overlaps the P3 region of the polyprotein ORF. Four related potyviruses infecting sweet potato (Ipomoea batatas) are predicted to contain a third ORF, called pispo, which overlaps the 3′ third of the P1 region. Recently, pipo has been shown to be expressed via polymerase slippage at a conserved GA6 sequence. Here, we show that pispo is also expressed via polymerase slippage at a GA6 sequence, with ...
Subjects
free text keywords: RNA virus, frameshift, FEATHERY MOTTLE VIRUS, CHLOROTIC-STUNT-VIRUS, RNA silencing suppression, DISTINCT SUPPRESSORS, PROTEIN DOMAINS, COMPLETE NUCLEOTIDE-SEQUENCE, Original Article, 1183 Plant biology, microbiology, virology, VIRAL SUPPRESSOR, STRUCTURE PREDICTION, Original Articles, overlapping gene, transcriptional slippage, HC-PRO, FAMILY POTYVIRIDAE, ARGONAUTE-BINDING, gene expression
Funded by
WT| Systematic Bioinformatic Discovery of 'Hidden' Virus Genes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 088789
  • Funding stream: Immunology and Infectious Disease ; Immune System in Health and Disease
,
WT| Encyclopedia of RNA Virus Elements: systematic bioinformatic discovery and experimental analysis of hidden genes, non-canonical translation mechanisms, and other functional elements in RNA virus genomes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 106207
  • Funding stream: Pathogen Biology and Disease Transmission ; Immunology and Infectious Disease
,
RCUK| Non-canonical gene expression: Investigating a novel stimulator and a novel function for ribosomal frameshifting
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: BB/J007072/1
  • Funding stream: BBSRC
,
RCUK| Deciphering the enigmatic expression mechanism of the newly discovered PIPO gene in the Potyviridae family of plant viruses
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: BB/J015652/1
  • Funding stream: BBSRC
67 references, page 1 of 5

Adams, M., Antoniw, J. and Fauquet, C. (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch. Virol. 150, 459–479. 15592889 [PubMed]

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410. 2231712 [PubMed]

Anandalakshmi, R., Pruss, G.J., Ge, X., Marathe, R., Mallory, A.C., Smith, T.H. and Vance, V.B. (1998) A viral suppressor of gene silencing in plants. Proc. Natl. Acad. S ci. USA, 95, 13 079–13 084. 9419317 [OpenAIRE] [PubMed]

Angermüller, C., Biegert, A. and Söding, J. (2012) Discriminative modelling of context‐specific amino acid substitution probabilities. Bioinformatics, 28, 3240–3247. 23080114 [PubMed]

Azevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., Braun, L., Bergdoll, M., Hakimi, M.A. and Lagrange, T. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen‐encoded GW repeat protein. Genes Dev. 24, 904–915. 20439431 [OpenAIRE] [PubMed]

Baumberger, N., Tsai, C.‐H., Lie, M., Havecker, E. and Baulcombe, D.C. (2007) The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609–1614. 17869110 [PubMed]

Brigneti, G., Voinnet, O., Li, W.X., Ji, L.H., Ding, S.W. and Baulcombe, D.C. (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana . EMBO J. 17, 6739–6746. 9822616 [OpenAIRE] [PubMed]

Chung, B.Y.‐W., Miller, W.A., Atkins, J.F. and Firth, A.E. (2008) An overlapping essential gene in the Potyviridae. Proc. Natl. Acad. Sci. USA, 105, 5897–5902. 18408156 [OpenAIRE] [PubMed]

Clark, C.A., Davis, J.A., Abad, J.A., Cuellar, W.J., Fuentes, S., Kreuze, J.F., Gibson, R.W., Mukasa, S.B., Tugume, A.K. and Tairo, F.D. (2012) Sweetpotato viruses: 15 years of progress on understanding and managing complex diseases. Plant Dis. 96, 168–185.

Cuellar, W.J., Kreuze, J.F., Rajamäki, M.‐L., Cruzado, K.R., Untiveros, M. and Valkonen, J.P. (2009) Elimination of antiviral defense by viral RNase III. Proc. Natl. Acad. Sci. USA, 106, 10 354–10 358. 19118191 [OpenAIRE] [PubMed]

El‐Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M.‐A., Jacobsen, S.E., Cooke, R. and Lagrange, T. (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE‐binding platforms in R NAi‐related components. Genes Dev. 21, 2539–2544. 17938239 [OpenAIRE] [PubMed]

Fang, Y., Treffers, E.E., Li, Y., Tas, A., Sun, Z., van der Meer, Y., de Ru, A.H., van Veelen, P.A., Atkins, J.F. and Snijder, E.J. (2012) Efficient −2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. USA, 109, E2920–E2928. 23043113 [OpenAIRE] [PubMed]

Firth, A.E. (2014) Mapping overlapping functional elements embedded within the protein‐coding regions of RNA viruses. Nucleic Acids Res. 42, 12 425–12 439.

Firth, A.E. and Brierley, I. (2012) Non‐canonical translation in RNA viruses. J. Gen. Virol. 93, 1385–1409. 22535777 [OpenAIRE] [PubMed]

Gibson, R.W., Aritua, V., Byamukama, E., Mpembe, I. and Kayongo, J. (2004) Control strategies for sweet potato virus disease in Africa. Virus Res. 100, 115–122. 15036842 [PubMed]

67 references, page 1 of 5
Abstract
The single-stranded, positive-sense RNA genome of viruses in the genus Potyvirus encodes a large polyprotein that is cleaved to yield 10 mature proteins. The first three cleavage products are P1, HCpro and P3. An additional short open reading frame (ORF), called pipo, overlaps the P3 region of the polyprotein ORF. Four related potyviruses infecting sweet potato (Ipomoea batatas) are predicted to contain a third ORF, called pispo, which overlaps the 3′ third of the P1 region. Recently, pipo has been shown to be expressed via polymerase slippage at a conserved GA6 sequence. Here, we show that pispo is also expressed via polymerase slippage at a GA6 sequence, with ...
Subjects
free text keywords: RNA virus, frameshift, FEATHERY MOTTLE VIRUS, CHLOROTIC-STUNT-VIRUS, RNA silencing suppression, DISTINCT SUPPRESSORS, PROTEIN DOMAINS, COMPLETE NUCLEOTIDE-SEQUENCE, Original Article, 1183 Plant biology, microbiology, virology, VIRAL SUPPRESSOR, STRUCTURE PREDICTION, Original Articles, overlapping gene, transcriptional slippage, HC-PRO, FAMILY POTYVIRIDAE, ARGONAUTE-BINDING, gene expression
Funded by
WT| Systematic Bioinformatic Discovery of 'Hidden' Virus Genes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 088789
  • Funding stream: Immunology and Infectious Disease ; Immune System in Health and Disease
,
WT| Encyclopedia of RNA Virus Elements: systematic bioinformatic discovery and experimental analysis of hidden genes, non-canonical translation mechanisms, and other functional elements in RNA virus genomes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 106207
  • Funding stream: Pathogen Biology and Disease Transmission ; Immunology and Infectious Disease
,
RCUK| Non-canonical gene expression: Investigating a novel stimulator and a novel function for ribosomal frameshifting
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: BB/J007072/1
  • Funding stream: BBSRC
,
RCUK| Deciphering the enigmatic expression mechanism of the newly discovered PIPO gene in the Potyviridae family of plant viruses
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: BB/J015652/1
  • Funding stream: BBSRC
67 references, page 1 of 5

Adams, M., Antoniw, J. and Fauquet, C. (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch. Virol. 150, 459–479. 15592889 [PubMed]

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410. 2231712 [PubMed]

Anandalakshmi, R., Pruss, G.J., Ge, X., Marathe, R., Mallory, A.C., Smith, T.H. and Vance, V.B. (1998) A viral suppressor of gene silencing in plants. Proc. Natl. Acad. S ci. USA, 95, 13 079–13 084. 9419317 [OpenAIRE] [PubMed]

Angermüller, C., Biegert, A. and Söding, J. (2012) Discriminative modelling of context‐specific amino acid substitution probabilities. Bioinformatics, 28, 3240–3247. 23080114 [PubMed]

Azevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., Braun, L., Bergdoll, M., Hakimi, M.A. and Lagrange, T. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen‐encoded GW repeat protein. Genes Dev. 24, 904–915. 20439431 [OpenAIRE] [PubMed]

Baumberger, N., Tsai, C.‐H., Lie, M., Havecker, E. and Baulcombe, D.C. (2007) The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609–1614. 17869110 [PubMed]

Brigneti, G., Voinnet, O., Li, W.X., Ji, L.H., Ding, S.W. and Baulcombe, D.C. (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana . EMBO J. 17, 6739–6746. 9822616 [OpenAIRE] [PubMed]

Chung, B.Y.‐W., Miller, W.A., Atkins, J.F. and Firth, A.E. (2008) An overlapping essential gene in the Potyviridae. Proc. Natl. Acad. Sci. USA, 105, 5897–5902. 18408156 [OpenAIRE] [PubMed]

Clark, C.A., Davis, J.A., Abad, J.A., Cuellar, W.J., Fuentes, S., Kreuze, J.F., Gibson, R.W., Mukasa, S.B., Tugume, A.K. and Tairo, F.D. (2012) Sweetpotato viruses: 15 years of progress on understanding and managing complex diseases. Plant Dis. 96, 168–185.

Cuellar, W.J., Kreuze, J.F., Rajamäki, M.‐L., Cruzado, K.R., Untiveros, M. and Valkonen, J.P. (2009) Elimination of antiviral defense by viral RNase III. Proc. Natl. Acad. Sci. USA, 106, 10 354–10 358. 19118191 [OpenAIRE] [PubMed]

El‐Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M.‐A., Jacobsen, S.E., Cooke, R. and Lagrange, T. (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE‐binding platforms in R NAi‐related components. Genes Dev. 21, 2539–2544. 17938239 [OpenAIRE] [PubMed]

Fang, Y., Treffers, E.E., Li, Y., Tas, A., Sun, Z., van der Meer, Y., de Ru, A.H., van Veelen, P.A., Atkins, J.F. and Snijder, E.J. (2012) Efficient −2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. USA, 109, E2920–E2928. 23043113 [OpenAIRE] [PubMed]

Firth, A.E. (2014) Mapping overlapping functional elements embedded within the protein‐coding regions of RNA viruses. Nucleic Acids Res. 42, 12 425–12 439.

Firth, A.E. and Brierley, I. (2012) Non‐canonical translation in RNA viruses. J. Gen. Virol. 93, 1385–1409. 22535777 [OpenAIRE] [PubMed]

Gibson, R.W., Aritua, V., Byamukama, E., Mpembe, I. and Kayongo, J. (2004) Control strategies for sweet potato virus disease in Africa. Virus Res. 100, 115–122. 15036842 [PubMed]

67 references, page 1 of 5
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publication . Article . 2015

A novel sweet potato potyvirus open reading frame (ORF) is expressed via polymerase slippage and suppresses RNA silencing

Untiveros, Milton; Olspert, Allan; Artola, Katrin; Firth, Andrew E.; Kreuze, Jan F.; Valkonen, Jari P. T.;