Skip to main content
Top
Published in: Archives of Virology 6/2014

01-06-2014 | Original Article

Sequence variability in the HC-Pro coding regions of Korean soybean mosaic virus isolates is associated with differences in RNA silencing suppression

Authors: Mei-Jia Li, Jung-Kyu Kim, Eun-Young Seo, Seok Myeong Hong, Eui-Il Hwang, Jung-Kyung Moon, Leslie L. Domier, John Hammond, Young-Nam Youn, Hyoun-Sub Lim

Published in: Archives of Virology | Issue 6/2014

Login to get access

Abstract

Soybean mosaic virus (SMV), a member of the family Potyviridae, is an important viral pathogen affecting soybean production in Korea. Variations in helper component proteinase (HC-Pro) sequences and the pathogenicity of SMV samples from seven Korean provinces were compared with those of previously characterized SMV isolates from China, Korea and the United States. Phylogenetic analysis separated 16 new Korean SMV isolates into two groups. Fourteen of the new Korean SMV samples belonged to group II and were very similar to U.S. strain SMV G7 and Chinese isolate C14. One isolate in group II, A297-13, differed at three amino acid positions (L54F, N286D, D369N) in the HC-Pro coding sequence from severe isolates and SMV 413, showed very weak silencing suppressor activity, and produced only mild symptoms in soybean. To test the role of each amino acid substitution in RNA silencing and viral RNA accumulation, a series of point mutations was constructed. Substitution of N for D at position 286 in HC-Pro of SMV A297-12 significantly reduced silencing suppression activity. When the mutant HC-Pro of A297-13 was introduced into an infectious clone of SMV 413, accumulation of viral RNA was reduced to less than 3 % of the level of SMV 413 containing HC-Pro of A297-12 at 10 days post-inoculation (dpi) but increased to 40 % of SMV 413(HC-Pro A297-12) at 40 dpi. At 50 dpi RNA accumulation of SMV 413(HC-Pro A297-13) was similar to that of SMV 413(HC-Pro A297-12). However, at 50 dpi, the D at position 286 of HC-Pro in SMV 413(HC-Pro A297-13) was found to have reverted to N. The results showed that 1) a naturally occurring mutation in HC-Pro significantly reduced silencing suppression activity and accumulation of transgene and viral RNAs, and 2) that there was strong selection for revision to wild type when the mutation was introduced into an infectious clone of SMV.
Appendix
Available only for authorised users
Literature
1.
go back to reference Anjos JR, Jarlfors U, Ghabrial SA (1992) Soybean mosaic potyvirus enhances the titer of two comoviruses in dually infected soybean plants. Phytopathology 82:1022–1027CrossRef Anjos JR, Jarlfors U, Ghabrial SA (1992) Soybean mosaic potyvirus enhances the titer of two comoviruses in dually infected soybean plants. Phytopathology 82:1022–1027CrossRef
2.
go back to reference Arguello-Astorga G, Ascencio-Ibáñez JT, Dallas MB, Orozco BM, Hanley-Bowdoin L (2007) High-frequency reversion of geminivirus replication protein mutants during infection. J Virol 81:11005–11015PubMedCentralPubMedCrossRef Arguello-Astorga G, Ascencio-Ibáñez JT, Dallas MB, Orozco BM, Hanley-Bowdoin L (2007) High-frequency reversion of geminivirus replication protein mutants during infection. J Virol 81:11005–11015PubMedCentralPubMedCrossRef
3.
go back to reference Atreya CD, Pirone TP (1993) Mutational analysis of the helper component-proteinase gene of a potyvirus: effects of amino acid substitutions, deletions, and gene replacement on virulence and aphid transmissibility. Proc Natl Acad Sci USA 90:11919–11923PubMedCentralPubMedCrossRef Atreya CD, Pirone TP (1993) Mutational analysis of the helper component-proteinase gene of a potyvirus: effects of amino acid substitutions, deletions, and gene replacement on virulence and aphid transmissibility. Proc Natl Acad Sci USA 90:11919–11923PubMedCentralPubMedCrossRef
4.
go back to reference Atreya CD, Raccah B, Pirone TP (1990) A point mutation in the coat protein abolish aphid transmissibility of a potyvirus. Virology 178(1):161–165PubMedCrossRef Atreya CD, Raccah B, Pirone TP (1990) A point mutation in the coat protein abolish aphid transmissibility of a potyvirus. Virology 178(1):161–165PubMedCrossRef
5.
go back to reference Atsumi G, Nakahara KS, Wada TS, Choi SH, Masuta C, Uyeda I (2012) Heterologous expression of viral suppressors of RNA silencing complements virulence of the HC-Pro mutant of clover yellow vein virus in pea. Arch Virol 157:1019–1028PubMedCrossRef Atsumi G, Nakahara KS, Wada TS, Choi SH, Masuta C, Uyeda I (2012) Heterologous expression of viral suppressors of RNA silencing complements virulence of the HC-Pro mutant of clover yellow vein virus in pea. Arch Virol 157:1019–1028PubMedCrossRef
6.
go back to reference Bayne EH, Rakitina DV, Morozov SY, Baulcombe DC (2005) Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J 44:471–482PubMedCrossRef Bayne EH, Rakitina DV, Morozov SY, Baulcombe DC (2005) Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J 44:471–482PubMedCrossRef
7.
go back to reference Blanc S, Lopez-Moya JJ, Wang R, Garcia-Lampasona S, Thornbury DW, Pirone TP (1997) A specific interaction between coat protein and helper component correlates with aphid transmission of a potyvirus. Virology 231:141–147PubMedCrossRef Blanc S, Lopez-Moya JJ, Wang R, Garcia-Lampasona S, Thornbury DW, Pirone TP (1997) A specific interaction between coat protein and helper component correlates with aphid transmission of a potyvirus. Virology 231:141–147PubMedCrossRef
8.
go back to reference Blanc S, Ammar ED, Garcia-Lampasona S, Dolja VV, Llave C, Baker J, Pirone TP (1998) Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 79:3119–3122PubMed Blanc S, Ammar ED, Garcia-Lampasona S, Dolja VV, Llave C, Baker J, Pirone TP (1998) Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 79:3119–3122PubMed
9.
go back to reference Bragg JN, Jackson AO (2004) The C-terminal region of the Barley stripe mosaic virus γb protein participates in homologous interactions and is required for suppression of RNA silencing. Mol Plant Pathol 5:465–481PubMedCrossRef Bragg JN, Jackson AO (2004) The C-terminal region of the Barley stripe mosaic virus γb protein participates in homologous interactions and is required for suppression of RNA silencing. Mol Plant Pathol 5:465–481PubMedCrossRef
11.
go back to reference Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M (2007) pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana–virus interactions. Mol Plant Microbe Interact 20:740–750PubMedCrossRef Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M (2007) pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana–virus interactions. Mol Plant Microbe Interact 20:740–750PubMedCrossRef
12.
go back to reference Cho EK, Choi SH, Cho WT (1983) Newly recognized soybean mosaic virus mutants and sources of resistance in soybeans. Res Rep ORD (SPMU) 25:18–22 Cho EK, Choi SH, Cho WT (1983) Newly recognized soybean mosaic virus mutants and sources of resistance in soybeans. Res Rep ORD (SPMU) 25:18–22
13.
go back to reference Cho EK, Chung BJ (1976) Studies on identification and classification of soybean virus diseases I. Preliminary studies on a soybean virus disease. Korean J Plant Prot 15:61–68 Cho EK, Chung BJ (1976) Studies on identification and classification of soybean virus diseases I. Preliminary studies on a soybean virus disease. Korean J Plant Prot 15:61–68
14.
go back to reference Cho EK, Chung BJ, Lee SH (1977) Studies on identification and classification of soybean virus diseases in Korea. Etiology of a necrotic disease of Glycine max. Plant Dis Rep 61:313–317 Cho EK, Chung BJ, Lee SH (1977) Studies on identification and classification of soybean virus diseases in Korea. Etiology of a necrotic disease of Glycine max. Plant Dis Rep 61:313–317
15.
go back to reference Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467–470CrossRef Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467–470CrossRef
16.
go back to reference Cho EK, Goodman RM (1982) Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Sci 22:1133–1136CrossRef Cho EK, Goodman RM (1982) Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Sci 22:1133–1136CrossRef
17.
go back to reference Chung BJ, Lee SH, Cho EK, Park HC (1974) Identification of soybean viruses and soybean varietal reactions. Annu Rep Circ 26:137–145 Chung BJ, Lee SH, Cho EK, Park HC (1974) Identification of soybean viruses and soybean varietal reactions. Annu Rep Circ 26:137–145
18.
go back to reference Clarke DK, Duarte EA, Elena SF, Moya A, Dominigo E, Holland J (1994) The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci USA 91:4821–4824PubMedCentralPubMedCrossRef Clarke DK, Duarte EA, Elena SF, Moya A, Dominigo E, Holland J (1994) The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci USA 91:4821–4824PubMedCentralPubMedCrossRef
19.
go back to reference Deng M, Bragg JN, Ruzin S, Schichnes D, King D, Goodin MM, Jackson AO (2007) Role of the sonchus yellow net virus N protein in formation of nuclear viroplasms. J Virol 81:5362–5374PubMedCentralPubMedCrossRef Deng M, Bragg JN, Ruzin S, Schichnes D, King D, Goodin MM, Jackson AO (2007) Role of the sonchus yellow net virus N protein in formation of nuclear viroplasms. J Virol 81:5362–5374PubMedCentralPubMedCrossRef
20.
go back to reference Desbiez C, Girard M, Lecoq H (2010) A novel natural mutation in HC-Pro responsible for mild symptomatology of Zucchini yellow mosaic virus (ZYMV, Potyvirus) in cucurbits. Arch Virol 155:397–401PubMedCrossRef Desbiez C, Girard M, Lecoq H (2010) A novel natural mutation in HC-Pro responsible for mild symptomatology of Zucchini yellow mosaic virus (ZYMV, Potyvirus) in cucurbits. Arch Virol 155:397–401PubMedCrossRef
21.
go back to reference Dolja VV, Herndon KL, Pirone TP, Carrington JC (1993) Spontaneous mutagenesis of a plant potyvirus genome after insertion of a foreign gene. J Virol 67:5968–5975PubMedCentralPubMed Dolja VV, Herndon KL, Pirone TP, Carrington JC (1993) Spontaneous mutagenesis of a plant potyvirus genome after insertion of a foreign gene. J Virol 67:5968–5975PubMedCentralPubMed
22.
go back to reference Dombrovsky A, Sobolev I, Chejanovsky N, Raccah B (2007) Characterization of RR-1 and RR-2 cuticular proteins from Myzus persicae. Comp Biochem Physiol B 146:256–264PubMedCrossRef Dombrovsky A, Sobolev I, Chejanovsky N, Raccah B (2007) Characterization of RR-1 and RR-2 cuticular proteins from Myzus persicae. Comp Biochem Physiol B 146:256–264PubMedCrossRef
23.
go back to reference Domier LL, Hobbs HA, McCoppin NK, Bowen CR, Steinlage TA, Chang S, Wang Y, Hartman GL (2011) Multiple loci condition seed transmission of Soybean mosaic virus (SMV) and SMV-induced seed coat mottling in soybean. Phytopathology 101:750–756PubMedCrossRef Domier LL, Hobbs HA, McCoppin NK, Bowen CR, Steinlage TA, Chang S, Wang Y, Hartman GL (2011) Multiple loci condition seed transmission of Soybean mosaic virus (SMV) and SMV-induced seed coat mottling in soybean. Phytopathology 101:750–756PubMedCrossRef
24.
go back to reference Domier LL, Latorre IJ, Steinlage TA, McCoppin N, Hartman GL (2003) Variability and transmission by Aphis glycines of North American and Asian Soybean mosaic virus isolates. Arch Virol 148:1925–1941PubMedCrossRef Domier LL, Latorre IJ, Steinlage TA, McCoppin N, Hartman GL (2003) Variability and transmission by Aphis glycines of North American and Asian Soybean mosaic virus isolates. Arch Virol 148:1925–1941PubMedCrossRef
26.
go back to reference English JJ, Davenport GF, Elmayan T, Vaucheret H, Baulcombe DC (1997) Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J 12:597–603CrossRef English JJ, Davenport GF, Elmayan T, Vaucheret H, Baulcombe DC (1997) Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J 12:597–603CrossRef
27.
go back to reference Garcia-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6:225–232PubMedCrossRef Garcia-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6:225–232PubMedCrossRef
28.
go back to reference Govier DA, Kassanis B (1974) Evidence that a component other than the virus particle is needed for aphid transmission of potato virus Y. Virology 57:285–286PubMedCrossRef Govier DA, Kassanis B (1974) Evidence that a component other than the virus particle is needed for aphid transmission of potato virus Y. Virology 57:285–286PubMedCrossRef
29.
go back to reference Hajimorad MR, Eggenberger AL, Hill JH (2008) Adaptation of soybean mosaic virus avirulent chimeras containing P3 sequences from virulent strains to Rsv1-genotype soybeans is mediated by mutations in HC-Pro. Mol Plant Microbe Interact 21:937–946PubMedCrossRef Hajimorad MR, Eggenberger AL, Hill JH (2008) Adaptation of soybean mosaic virus avirulent chimeras containing P3 sequences from virulent strains to Rsv1-genotype soybeans is mediated by mutations in HC-Pro. Mol Plant Microbe Interact 21:937–946PubMedCrossRef
30.
go back to reference Huet H, Gal-On A, Meir E, Lecoq H, Raccah B (1994) Mutations in the helper component protease gene of zucchini yellow mosaic virus affect its ability to mediate aphid transmissibility. J Gen Virol 75:1407–1414PubMedCrossRef Huet H, Gal-On A, Meir E, Lecoq H, Raccah B (1994) Mutations in the helper component protease gene of zucchini yellow mosaic virus affect its ability to mediate aphid transmissibility. J Gen Virol 75:1407–1414PubMedCrossRef
31.
go back to reference Johansen LK, Carrington JC (2001) Silencing on the spot induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol 126:930–938PubMedCentralPubMedCrossRef Johansen LK, Carrington JC (2001) Silencing on the spot induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol 126:930–938PubMedCentralPubMedCrossRef
32.
go back to reference Johansen IE, Dougherty WG, Keller KE, Wang D, Hampton RO (1996) Multiple viral determinants affect seed transmission of pea seedborne mosaic virus in Pisum sativum. J Gen Virol 77:3149–3154PubMedCrossRef Johansen IE, Dougherty WG, Keller KE, Wang D, Hampton RO (1996) Multiple viral determinants affect seed transmission of pea seedborne mosaic virus in Pisum sativum. J Gen Virol 77:3149–3154PubMedCrossRef
33.
go back to reference Jossey S, Hobbs HA, Domier LL (2013) Role of soybean mosaic virus-encoded proteins in seed and aphid transmission in soybean. Phytopathology 103:941–948PubMedCrossRef Jossey S, Hobbs HA, Domier LL (2013) Role of soybean mosaic virus-encoded proteins in seed and aphid transmission in soybean. Phytopathology 103:941–948PubMedCrossRef
34.
go back to reference Kawakami S, Hori K, Hosokawa D, Okada Y, Watanabe Y (2003) Defective tobamovirus movement protein lacking wild-type phosphorylation sites can be complemented by substitutions found in revertants. J Virol 77:1452–1461PubMedCentralPubMedCrossRef Kawakami S, Hori K, Hosokawa D, Okada Y, Watanabe Y (2003) Defective tobamovirus movement protein lacking wild-type phosphorylation sites can be complemented by substitutions found in revertants. J Virol 77:1452–1461PubMedCentralPubMedCrossRef
35.
go back to reference Kim YH (2000) G7H, a new strain of soybean mosaic virus: its virulence and nucleotide sequence of cylindrical inclusion gene. Ph.D. thesis, Kyungpook National University, Daegu, p 120 Kim YH (2000) G7H, a new strain of soybean mosaic virus: its virulence and nucleotide sequence of cylindrical inclusion gene. Ph.D. thesis, Kyungpook National University, Daegu, p 120
36.
go back to reference Kim YH, Kim OS, Lee BC, Moon JK, Lee SC, Lee JY (2003) G7H, a new soybean mosaic virus strain: its virulence and nucleotide sequence of CI gene. Plant Dis 87:1372–1375CrossRef Kim YH, Kim OS, Lee BC, Moon JK, Lee SC, Lee JY (2003) G7H, a new soybean mosaic virus strain: its virulence and nucleotide sequence of CI gene. Plant Dis 87:1372–1375CrossRef
37.
go back to reference Lim SM (1985) Resistance to soybean mosaic virus in soybeans. Phytopathology 75:199–201CrossRef Lim SM (1985) Resistance to soybean mosaic virus in soybeans. Phytopathology 75:199–201CrossRef
38.
go back to reference Lim HS, Jang C, Bae H, Kim J, Lee C, Hong J, Ju H, Kim H, Domier LL (2011) Soybean mosaic virus infection and helper component-protease enhance accumulation of bean pod mottle virus-specific siRNAs. Plant Pathol J 27:315–323CrossRef Lim HS, Jang C, Bae H, Kim J, Lee C, Hong J, Ju H, Kim H, Domier LL (2011) Soybean mosaic virus infection and helper component-protease enhance accumulation of bean pod mottle virus-specific siRNAs. Plant Pathol J 27:315–323CrossRef
39.
go back to reference Lin SS, Wu HW, Jan FJ, Hou RF, Yeh SD (2007) Modifications of the helper component-protease of Zucchini yellow mosaic virus for generation of attenuated mutants for cross protection against severe infection. Phytopathology 97:287–296PubMedCrossRef Lin SS, Wu HW, Jan FJ, Hou RF, Yeh SD (2007) Modifications of the helper component-protease of Zucchini yellow mosaic virus for generation of attenuated mutants for cross protection against severe infection. Phytopathology 97:287–296PubMedCrossRef
40.
go back to reference Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, Garcia-Arenal F (2002) The rate and character of spontaneous mutation in an RNA virus. Genetics 162:1505–1511PubMedCentralPubMed Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, Garcia-Arenal F (2002) The rate and character of spontaneous mutation in an RNA virus. Genetics 162:1505–1511PubMedCentralPubMed
41.
go back to reference Moya A, Elena SF, Bracho A, Miralles R, Barrio E (2000) The evolution of RNA viruses: a population genetics view. Proc Natl Acad Sci USA 97:6967–6973PubMedCentralPubMedCrossRef Moya A, Elena SF, Bracho A, Miralles R, Barrio E (2000) The evolution of RNA viruses: a population genetics view. Proc Natl Acad Sci USA 97:6967–6973PubMedCentralPubMedCrossRef
42.
go back to reference Peng YH, Kadoury D, Gal-On A, Huet H, Wang Y, Raccah B (1998) Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions. J Gen Virol 79:897–904PubMed Peng YH, Kadoury D, Gal-On A, Huet H, Wang Y, Raccah B (1998) Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions. J Gen Virol 79:897–904PubMed
43.
go back to reference Petty IT, Hunter BG, Wei N, Jackson AO (1989) Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology 171:342–349PubMedCrossRef Petty IT, Hunter BG, Wei N, Jackson AO (1989) Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology 171:342–349PubMedCrossRef
44.
go back to reference Pruss G, Ge X, Shi XM, Carrington JC, Vance VB (1997) Plant vira1 synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–868PubMedCentralPubMedCrossRef Pruss G, Ge X, Shi XM, Carrington JC, Vance VB (1997) Plant vira1 synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–868PubMedCentralPubMedCrossRef
45.
go back to reference Rajamäki M, Merits A, Rabenstein F, Andrejeva J, Paulin L, Kekarainen T, Kreuze JF, Forster RL, Valkonen JP (1998) Biological, serological, and molecular differences among isolates of potato a potyvirus. Phytopathology 88:311–321PubMedCrossRef Rajamäki M, Merits A, Rabenstein F, Andrejeva J, Paulin L, Kekarainen T, Kreuze JF, Forster RL, Valkonen JP (1998) Biological, serological, and molecular differences among isolates of potato a potyvirus. Phytopathology 88:311–321PubMedCrossRef
46.
go back to reference Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:283–295PubMedCrossRef Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:283–295PubMedCrossRef
48.
go back to reference Shi XM, Miller H, Verchot J, Carrington JC, Vance VB (1997) Mutations in the region encoding the central domain of helper component-proteinase (HC-Pro) eliminate potato virus X/potyviral synergism. Virology 231:35–42PubMedCrossRef Shi XM, Miller H, Verchot J, Carrington JC, Vance VB (1997) Mutations in the region encoding the central domain of helper component-proteinase (HC-Pro) eliminate potato virus X/potyviral synergism. Virology 231:35–42PubMedCrossRef
49.
go back to reference Tamura K, Peterson D, Perterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRef Tamura K, Peterson D, Perterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRef
50.
go back to reference Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882PubMedCentralPubMedCrossRef Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882PubMedCentralPubMedCrossRef
51.
go back to reference Torres-Barceló C, Martín S, Darós JA, Elena SF (2008) From hypo- to hypersuppression: effect of amino acid substitutions on the RNA-silencing suppressor activity of the Tobacco etch potyvirus HC-Pro. Genetics 180:1039–1049PubMedCentralPubMedCrossRef Torres-Barceló C, Martín S, Darós JA, Elena SF (2008) From hypo- to hypersuppression: effect of amino acid substitutions on the RNA-silencing suppressor activity of the Tobacco etch potyvirus HC-Pro. Genetics 180:1039–1049PubMedCentralPubMedCrossRef
52.
go back to reference Vaira AM, Lim H-S, Bauchan GR, Owens RA, Natilla A, Dienelt MM, Reinsel MD, Hammond J (2012) Lolium latent virus (Alphaflexiviridae) coat proteins: expression and functions in infected plant tissue. J Gen Virol 93:1814–1824PubMedCrossRef Vaira AM, Lim H-S, Bauchan GR, Owens RA, Natilla A, Dienelt MM, Reinsel MD, Hammond J (2012) Lolium latent virus (Alphaflexiviridae) coat proteins: expression and functions in infected plant tissue. J Gen Virol 93:1814–1824PubMedCrossRef
53.
go back to reference Varrelmann M, Maiss E, Pilot R, Palkovics L (2007) Use of pentapeptide-insertion scanning mutagenesis for functional mapping of the plum pox virus helper component proteinase suppressor of gene silencing. J Gen Virol 88:1005–1015PubMedCrossRef Varrelmann M, Maiss E, Pilot R, Palkovics L (2007) Use of pentapeptide-insertion scanning mutagenesis for functional mapping of the plum pox virus helper component proteinase suppressor of gene silencing. J Gen Virol 88:1005–1015PubMedCrossRef
54.
go back to reference Wu HW, Lin SS, Chen KC, Yeh SD, Chua NH (2010) Discriminating mutations of HC-Pro of Zucchini yellow mosaic virus with differential effects on small RNA pathways involved in viral pathogenicity and symptom development. Mol Plant Microbe Interact 23:17–28PubMedCrossRef Wu HW, Lin SS, Chen KC, Yeh SD, Chua NH (2010) Discriminating mutations of HC-Pro of Zucchini yellow mosaic virus with differential effects on small RNA pathways involved in viral pathogenicity and symptom development. Mol Plant Microbe Interact 23:17–28PubMedCrossRef
55.
go back to reference Wurch T, Lestienne F, Pauwels P (1998) A modified overlap extension PCR method to create chimeric genes in the absence of restriction enzymes. Biotechnol Tech 12:653–657CrossRef Wurch T, Lestienne F, Pauwels P (1998) A modified overlap extension PCR method to create chimeric genes in the absence of restriction enzymes. Biotechnol Tech 12:653–657CrossRef
56.
go back to reference Yambao MLM, Yagihashi H, Sekiguchi H, Sekiguchi T, Sasaki T, Sato M, Atsumi G, Tacahashi Y, Nakahara KS, Uyeda I (2008) Point mutations in helper component protease of clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean. Arch Virol 153:105–115PubMedCrossRef Yambao MLM, Yagihashi H, Sekiguchi H, Sekiguchi T, Sasaki T, Sato M, Atsumi G, Tacahashi Y, Nakahara KS, Uyeda I (2008) Point mutations in helper component protease of clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean. Arch Virol 153:105–115PubMedCrossRef
57.
go back to reference Yang S, Ravelonandro M (2002) Molecular studies of the synergistic interactions between plum pox virus HC-Pro protein and potato virus X. Arch Virol 147:2301–2312PubMedCrossRef Yang S, Ravelonandro M (2002) Molecular studies of the synergistic interactions between plum pox virus HC-Pro protein and potato virus X. Arch Virol 147:2301–2312PubMedCrossRef
58.
go back to reference Xu Z, Polston JE, Goodman RM (1986) Identification of soybean mosaic, southern bean mosaic and tobacco ringspot viruses from soybean in the People’s Republic of China. Ann Appl Biol 108:51–57CrossRef Xu Z, Polston JE, Goodman RM (1986) Identification of soybean mosaic, southern bean mosaic and tobacco ringspot viruses from soybean in the People’s Republic of China. Ann Appl Biol 108:51–57CrossRef
59.
go back to reference Zhang CQ, Ghabrial SA (2006) Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344:401–411PubMedCrossRef Zhang CQ, Ghabrial SA (2006) Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344:401–411PubMedCrossRef
Metadata
Title
Sequence variability in the HC-Pro coding regions of Korean soybean mosaic virus isolates is associated with differences in RNA silencing suppression
Authors
Mei-Jia Li
Jung-Kyu Kim
Eun-Young Seo
Seok Myeong Hong
Eui-Il Hwang
Jung-Kyung Moon
Leslie L. Domier
John Hammond
Young-Nam Youn
Hyoun-Sub Lim
Publication date
01-06-2014
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 6/2014
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-013-1964-4

Other articles of this Issue 6/2014

Archives of Virology 6/2014 Go to the issue