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Efficient dsRNA-mediated transgenic resistance to Beet necrotic yellow vein virus in sugar beets is not affected by other soilborne and aphid-transmitted viruses

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Abstract

Rhizomania caused by Beet necrotic yellow vein virus (BNYVV) is one of the most devastating sugar beet diseases. Sugar beet plants engineered to express a 0.4 kb inverted repeat construct based on the BNYVV replicase gene accumulated the transgene mRNA to similar levels in leaves and roots, whereas accumulation of the transgene-homologous siRNA was more pronounced in roots. The roots expressed high levels of resistance to BNYVV transmitted by the vector, Polymyxa betae. Resistance to BNYVV was not decreased following co-infection of the plants with Beet soil borne virus and Beet virus Q that share the same vector with BNYVV. Similarly, co-infection with the aphid-transmitted Beet mild yellowing virus, Beet yellows virus (BYV), or with all of the aforementioned viruses did not affect the resistance to BNYVV, while they accumulated in roots. These viruses are common in most of the sugar beet growing areas in Europe and world wide. However, there was a competitive interaction between BYV and BMYV in sugar beet leaves, as infection with BYV decreased the titres of BMYV. Other interactions between the viruses studied were not observed. The results suggest that the engineered resistance to BNYVV expressed in the sugar beets of this study is efficient in roots and not readily compromised following infection of the plants with heterologous viruses.

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References

  • Abe H, Tamada T (1986) Association of beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Ann Phytopath Soc Japan 52:235–247

    Google Scholar 

  • Andika IB, Kondo H, Tamada T (2005) Evidence that RNA silencing-mediated resistance to Beet necrotic yellow vein virus is less effective in roots than in leaves. Mol Plant Microbe Interact 18:194–204

    Article  PubMed  CAS  Google Scholar 

  • Andika IB, Kondo H, Rahim MD, Tamada T (2006) Lower levels of transgene silencing in roots is associated with reduced DNA methylation levels at non-symmetrical sites but not at symmetrical sites. Plant Mol Biol 60:423–435

    Article  PubMed  CAS  Google Scholar 

  • Biancardi E, Lewellen RT, De Biaggi M, Erichsen AW, Stevanato P (2002) The origin of rhizomania resistance in sugar beet. Euphytica 127:383–397

    Article  CAS  Google Scholar 

  • Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483

    PubMed  CAS  Google Scholar 

  • De Biaggi M (1987) Methodes de selection – un cas concret. In: Proceedings of the 50th IIRB Winter Congress. vol II, Brussels, pp 157–163

  • Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68–71

    Article  PubMed  CAS  Google Scholar 

  • Di Nicola-Negri E, Brunetti A, Tavazza M, Ilardi V (2005) Hairpin RNA-mediated silencing of Plum pox virus P1 and HC-Pro genes for efficient and predictable resistance to the virus. Transgenic Res 14:989–994

    Article  PubMed  CAS  Google Scholar 

  • Dunoyer P, Pfeffer S, Fritsch C, Hemmer O, Voinnet O, Richards KE (2002) Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J 29:555–567

    Article  PubMed  CAS  Google Scholar 

  • Fuentes A, Ramos PL, Fiallo E, Callard D, Sanchez Y, Peral R, Rodriguez R, Pujol M (2006) Intron-hairpin RNA derived from replication associated protein C1 gene confers immunity to Tomato yellow leaf curl virus infection in transgenic tomato plants. Transgenic Res 15:291–304

    Article  PubMed  CAS  Google Scholar 

  • Germundsson A, Sandgren M, Barker H, Savenkov EI, Valkonen JPT (2002) Initial infection of roots and leaves reveals different resistance phenotypes associated with coat protein gene-mediated resistance to Potato mop-top virus. J Gen Virol 83:1201–1209

    PubMed  CAS  Google Scholar 

  • Gidner S, Lennefors B-L, Nilsson N-O, Bensefelt J, Johansson E, Gyllenspetz U, Kraft T (2005) QTL mapping of BNYVV resistance from the WB41 source in sugar beet. Genome 48:279–285

    PubMed  CAS  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in post transcriptional gene silencing. Science 286:950–952

    Article  PubMed  CAS  Google Scholar 

  • Hehn A, Fritsch C, Richards KE, Guilley H, Jonard G (1997) Evidence for in vitro and in vivo autocatalytic processing of the primary translation product of beet necrotic yellow vein virus RNA 1 by a papain-like proteinase. Arch Virol 142:1051–1058

    Article  PubMed  CAS  Google Scholar 

  • Heijbroek W, Musters PMS, Schoone AHL (1999) Variation in pathogenicity and multiplication of beet necrotic yellow vein virus (BNYVV) in relation to the resistance of sugar-beet cultivars. Eur J Plant Pathol 105:397–405

    Article  Google Scholar 

  • Ivanović M, Macfarlane I. Woods RD (1982) In: Annual Report of Rothamsted Experimental Station for 1982, pp 189–190

  • Joersbo M, Donaldson I, Kreiberg J, Guldager Petersen S, Brunstedt J, Okkels FT (1998) Analysis of mannose selection used for transformation of sugar beet. Mol Breed 4:111–117

    Article  CAS  Google Scholar 

  • Johansen LK, Carrington JC (2001) Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol 126:930–938

    Article  PubMed  CAS  Google Scholar 

  • Kaniewski W, Lawson C (1998) Coat protein and replicase-mediated resistance to plant viruses. In: Hadidi A, Khetarpal RK, Koganezawa H (eds) Plant Virus Disease Control. APS Press, St. Paul, Minnesota, USA, pp 65–78

    Google Scholar 

  • Kiguchi T, Saito M, Tamada T (1996) Nucleotide sequence analysis of RNA-5 of five isolates of beet necrotic yellow vein virus and the identity of a deletion mutant. J Gen Virol 77:575–580

    PubMed  CAS  Google Scholar 

  • Koenig R, Beier C, Commandeur U, Lüth U, Kaufmann A, Lüddecke P (1996) Beet soil-borne virus RNA3 – a further example of the heterogeneity of the gene content of furovirus genomes and of triple gene block-carrying RNAs. Virology 216:202–207

    Article  PubMed  CAS  Google Scholar 

  • Koenig R, Haeberle AM, Commandeur U (1997) Detection and characterization of a distinct type of beet necrotic yellow vein virus RNA 5 in a sugarbeet growing area in Europe. Arch Virol 142:1499–1504

    Article  PubMed  CAS  Google Scholar 

  • Koenig R, Lüddecke P, Haeberlé AM (1995) Detection of beet necrotic yellow vein virus strains, variants and mixed infections by examining single-strand conformation polymorphisms of immunocapture RT-PCR products. J Gen Virol 76:2051–2055

    PubMed  CAS  Google Scholar 

  • Koenig R, Pleij CWA, Beier C, Commandeur U (1998) Genome properties of beet virus Q, a new furo-like virus from sugarbeet, determined from unpurified virus. J Gen Virol 79:2027–2036

    PubMed  CAS  Google Scholar 

  • Koenig R, Pleij CWA, Büttner G (2000) Structure and variability of the 3′ end of RNA 3 of beet soil-borne pomovirus – a virus with uncertain pathogenic effects. Arch Virol 145:1173–1181

    Article  PubMed  CAS  Google Scholar 

  • Kreuze JF, Savenkov EI, Li X, Cuellar W, Valkonen JPT (2005) Viral class 1 RNaseIII involved in suppression of RNA silencing. J Virol 79:7227–7238

    Article  PubMed  CAS  Google Scholar 

  • Kruse M, Koenig R, Hoffmann A, Kaufmann A, Commandeur U, Solovyev AG, Savenkov EI, Burgermeister W (1994) Restriction fragment length polymorphism analysis of reverse transcription-PCR products reveals the existence of two major strain groups of beet necrotic yellow vein virus. J Gen Virol 75:1835–1842

    PubMed  CAS  Google Scholar 

  • Lennefors BL, Savenkov EI, Mukasa SB, Valkonen JPT (2005) Sequence divergence of four soil-borne sugarbeet-infecting viruses. Virus Genes 31:57–64

    Article  PubMed  CAS  Google Scholar 

  • Lennefors B-L, Savenkov EI, Bensefelt J, Wremerth-Weich E, van Roggen P, Tuvesson S, Valkonen JPT, Gielen J (2006) dsRNA-mediated resistance to Beet necrotic yellow vein virus infections in sugar beet (Beta vulgaris L. ssp. vulgaris). Mol Breed 18:313–325

    Article  CAS  Google Scholar 

  • Lewellen RT, Skoyen IO, Erichsen AW (1987) Breeding sugar beet for resistance to rhizomania: Evaluation of host-plant reactions and selection for and inheritance of resistance. In: Proceedings of the 50th IIRB Winter Congress, February 1987, vol II. Brussels, pp 139–156

  • Link D, Schmidlin L, Schirmer A, Klein E, Erhardt M, Geldreich A, Lemaire O, Gilmer D (2005) Functional characterization of Beet necrotic yellow vein virus RNA-5-encoded p26 protein: evidence for structural pathogenicity determinants. J Gen Virol 86:2115–2125

    Article  PubMed  CAS  Google Scholar 

  • Liu H-Y, Sears JL, Lewellen RT (2005) Occurrence of resistance-breaking Beet necrotic yellow vein virus of sugar beet. Plant Dis 89:464–468

    Article  CAS  Google Scholar 

  • Medina V, Peremyslov VV, Hagiwara Y, Dolja VV (1999) Subcellular localization of the HSP70-homolog encoded by beet yellows closterovirus. Virology 260:173–181

    Article  PubMed  CAS  Google Scholar 

  • Meunier A, Schmit JF, Stas A, Kutluk N, Bragard C (2003) Multiplex reverse transcription-PCR for simultaneous detection of Beet necrotic yellow vein virus, Beet soilborne virus, and Beet virus Q and their vector Polymyxa betae KESKIN on sugar beet. Appl Environ Microbiol 69:2356–2360

    Article  PubMed  CAS  Google Scholar 

  • Mitter N, Sulistyowati E, Dietzgen RG (2003) Cucumber mosaic virus infection transiently breaks dsRNA-induced transgenic immunity to Potato virus Y in tobacco. Mol Plant-Microbe Interact 16:936–944

    Article  PubMed  CAS  Google Scholar 

  • Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, Hemmer O, Kretsch T, Richards KE, Genschik P, Ziegler-Graff V (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. PNAS 103:1994–1999

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer S, Dunoyer P, Heim F, Richards KE, Jonard G, Ziegler-Graff V (2002) P0 of Beet western yellows virus is a suppressor of posttranscriptional gene silencing. J Virol 13:6815–6824

    Article  CAS  Google Scholar 

  • Powell-Abel P, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT, Beachy RN (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–743

    Article  Google Scholar 

  • Reed JC, Kasschau KD, Prokhnevsky AI, Gopinath K, Pogue GP, Carrington JC, Dolja VV (2003) Suppressor of RNA silencing encoded by Beet yellows virus. Virology 306:203–209

    Article  PubMed  CAS  Google Scholar 

  • Sanford JC, Johnston SA (1985) The concept of Parasite-Derived Resistance – Deriving Resistance Genes from the Parasite’s Own Genome. J Theor Biol 113:395–405

    Article  Google Scholar 

  • Savenkov EI, Valkonen JPT (2001) Coat protein gene-mediated resistance to Potato virus A in transgenic plants is suppressed following infection with another potyvirus. J Gen Virol 82:2275–2278

    PubMed  CAS  Google Scholar 

  • Schirmer A, Link D, Cognat V, Moury B, Beuve M, Meunier A, Bragard C, Gilmer D, Lemaire O (2005) Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. J Gen Virol 86:2897–2911

    Article  PubMed  CAS  Google Scholar 

  • Scholten OE, Jansen RC, Paul Keizer LC, De Bock TSM, Lange W (1996) Major genes for resistance to beet necrotic yellow vein virus (BNYVV) in Beta vulgaris. Euphytica 91:331–339

    Article  Google Scholar 

  • Smith HG (1991) Beet mild yellowing luteo virus. In: Brunt AH, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L (eds) Viruses of Plants, Cambrige, UK, pp 209–211

    Google Scholar 

  • Smith HG, Hallsworth PB (1990) The effects of yellowing viruses on yield of sugar beet in field trials, 1985 and 1987. Ann App Biol 116:503–511

    Article  Google Scholar 

  • Smith H, Karasev A (1991) Beet yellows closterovirus. In: Brunt AH, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L (eds) Viruses of Plants, Cambridge, UK, pp 227–230

    Google Scholar 

  • Smith NA, Singh SP, Wang MB, Stoutjesdijk PA, Green AG, Waterhouse PM (2000) Total silencing by intron-spliced hairpin RNAs. Nature 407:319–320

    Article  PubMed  CAS  Google Scholar 

  • Stas A, Meunier A, Schmit JF, Bragard C. (2001) First report of BVQ in Belgium. Plant Dis 85:1288

    Article  Google Scholar 

  • Stevens M, Asher MJC (2006) Preliminary investigations into the interactions between Beet mild yellowing virus (BMYV) and Beet necrotic yellow vein virus (BNYVV) in susceptible and rhizomania-resistant varieties. Aspects of Appl Biol 76:13–17

    Google Scholar 

  • Stevens M, Freeman B, Liu H-Y, Herrbach E, Lemaire O (2005a) Beet poleroviruses: close friends or distant relatives? Mol Plant Pathol 6:1–9

    Article  CAS  Google Scholar 

  • Stevens M, Patron NJ, Dolby CA, Weekes R, Hallsworth PB, Lemaire O, Smith HG (2005b) Distribution and properties of geographically distinct isolates of sugar beet yellowing viruses. Plant Pathol 54:100–107

    Article  CAS  Google Scholar 

  • Tamada T (1975) Beet necrotic yellow vein virus. In: C.M.I./A.A.B. Descriptions of Plant Viruses, No. 144, Perthshire, Scotland

  • Tamada T (1999) Benyvirus. In: Granoff A, Webster R (eds) Encyclopedia of Virology 2nd ed, Vol II Academic Press, New York, pp 154–160

    Google Scholar 

  • Tamada T, Baba T (1973) Beet necrotic yellow vein virus from rhizomania-affected sugar beet in Japan. Ann Phytopath Soc Japan 39:325–332

    Google Scholar 

  • Tomita R, Hamada T, Horiguchi G, Iba K, Kodama H (2004) Transgene overexpression with cognate small interfering RNA in tobacco. FEBS Lett 573:117–120

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nature Rev Genet 6:206–220

    Article  CAS  Google Scholar 

  • Waterhouse PM, Graham MW, Wang M-B (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. PNAS 95:13959–13964

    Article  PubMed  CAS  Google Scholar 

  • Waterhouse PM, Smith NA, Wang M-B (1999) Virus resistance and gene silencing: killing the messenger. Trends Plant Sci 11:452–457

    Article  Google Scholar 

  • Whitney ED (1989) Identification, distribution, and testing for resistance to Rhizomania in Beta maritima. Plant Dis 73:287–290

    Article  Google Scholar 

  • Wintermantel WM (2005) Co-infection of beet mosaic virus with beet yellowing viruses leads to increased symptom expression on sugar beet. Plant Dis 89:325–331

    Article  Google Scholar 

  • Ye K, Malinina L, Patel DJ (2003) Recognition of small interfering RNA by a viral suppressor of RNA-silencing. Nature 426:874–878

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Heléne Sandell, Gun Carlsson, Susann Lund, Kerstin Ahlgren and Gabriella Arndt for excellent technical assistance, Åsa Karlsson for careful greenhouse work, Maria Nihlgård, Stig Tuvesson, Jan Bensefelt and Elisabeth Wremerth-Weich for helpful discussions, Mark Stevens (Broom’s Barn Experimental Station, UK) for valuable materials, and Jan Gielen and Thomas Kraft for critically reading the manuscript.

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Authors and Affiliations

  1. Syngenta Seeds AB, Box 302, 261 23, Landskrona, Sweden

    Britt-Louise Lennefors, Petra M. van Roggen & Flemming Yndgaard

  2. Department of Plant Biology and Forest Genetics, Swedish University of Agricultural Sciences, Box 7080, 750 07, Uppsala, Sweden

    Eugene I. Savenkov & Jari P. T. Valkonen

  3. Department of Applied Biology, University of Helsinki, PO Box 27, 00014, Helsinki, Finland

    Jari P. T. Valkonen

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  1. Britt-Louise Lennefors
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  2. Petra M. van Roggen
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  3. Flemming Yndgaard
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  4. Eugene I. Savenkov
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  5. Jari P. T. Valkonen
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Correspondence to Jari P. T. Valkonen.

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Lennefors, BL., van Roggen, P.M., Yndgaard, F. et al. Efficient dsRNA-mediated transgenic resistance to Beet necrotic yellow vein virus in sugar beets is not affected by other soilborne and aphid-transmitted viruses. Transgenic Res 17, 219–228 (2008). https://doi.org/10.1007/s11248-007-9092-0

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  • DOI: https://doi.org/10.1007/s11248-007-9092-0

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