Achievements and prospects in breeding for rhizomania resistance in sugar beet

Field Crops Research

Volumn 122, Issue 3, 2011, Pages 165-172

  Pavli, Ourania I ^a   Stevanato, Piergiorgio ^b   Biancardi, Enrico ^c   Skaracis, George N ^a  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^b UNIVERSITY OF PADOVA   (Italy)

^c ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Beet necrotic yellow vein virus; Resistance breeding; Rhizomania resistance; Sugar beet

Indexed keywords

AGRICULTURAL ECONOMICS; BIOCONTROL AGENT; BIOLOGICAL CONTROL; BIOTECHNOLOGY; CROP YIELD; CULTIVAR; DISEASE RESISTANCE; DISEASE SEVERITY; FUTURE PROSPECT; GENETIC VARIATION; QUALITATIVE ANALYSIS; SUGAR BEET; VIRAL DISEASE;

BEET NECROTIC YELLOW VEIN VIRUS; BEET NECROTIC YELLOW VEIN VIRUS A; BETA VULGARIS SUBSP. VULGARIS; POLYMYXA; POLYMYXA BETAE; PROTOCTISTA;

EID: 79956089711     PISSN: 03784290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fcr.2011.03.019     Document Type: Review

References (107)

1. Abe H., Tamada T. Association of Beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Ann. Phytopathol. Soc. Jpn. 1986, 52:235-247.
2. Acosta-Leal R., Bryan B.K., Rush C.M. Host effect on the genetic diversification of Beet necrotic yellow vein virus single-plant populations. Phytopathology 2010, 100:1204-1212.
3. Acosta-Leal R., Bryan B.K., Smith J.T., Rush C.M. Breakdown of host resistance by independent evolutionary lineages of Beet necrotic yellow vein virus involves a parallel C/U mutation in its p25 gene. Phytopathology 2010, 100:127-133.
4. Acosta-Leal R., Fawley M.W., Rush C.M. Changes in the intraisolate genetic structure of Beet necrotic yellow vein virus populations associated with plant resistance breakdown. Virology 2008, 376:60-68.
5. Acosta-Leal R., Rush C.M. Mutations associated with resistance-breaking isolates of Beet necrotic yellow vein virus and their allelic discrimination using TaqMan technology. Phytopathology 2007, 97:325-330.
6. Amiri R., Moghaddam M., Mesbah M., Sadeghian S.Y., Ghannadha M.R., Izadpanah K. The inheritance of resistance to Beet necrotic yellow vein virus (BNYVV) in B. vulgaris subsp. maritima, accession WB42: statistical comparisons with Holly-1-4. Euphytica 2003, 132:363-373.
7. Andika I.B., Kondo H., Tamada T. Evidence that RNA silencing-mediated resistance to Beet necrotic yellow vein virus is less effective in roots than in leaves. MPMI 2005, 18:194-204.
8. Asher M.J.C., Grimmer M.K., Mutasa-Goettgens E.S. Selection and characterization of resistance to Polymyxa betae, vector of Beet necrotic yellow vein virus, derived from wild sea beet. Plant Pathol. 2009, 58:250-260.
9. Barr K.J., Asher M.J.C., Lewis B.G. Resistance to Polymyxa betae in wild Beta species. Plant Pathol. 1995, 44:301-307.
10. Barzen E., Rainer S., Fuchs E., Borchardt D.C., Salamini F. Development of coupling-repulsion-phase SCAR markers diagnostic for the sugar beet Rr1 allele conferring resistance to rhizomania. Mol. Breed. 1997, 3:231-238.
11. Baulcombe D. Viruses and gene silencing in plants. Arch. Virol. Suppl. 1999, 15:189-201.
12. Beachy R.N., Loesch-Fries S., Tumer T.E. Coat protein-mediated resistance against virus infection. Ann. Rev. Phytopathol. 1990, 28:451-474.
13. Beck D.L., Van Dolleerd C.J., Lough T.J., Balmori E., Voot D.M., Andersen M.T., O'Brien I.E., Forster R.L.S. Disruption of virus movement confers broad spectrum resistance against systemic infection by plant viruses with a triple gene block. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10310-10314.
14. Biancardi E., Lewellen R.T., DeBiaggi M., Erichsen A.W., Stevanato P. The origin of rhizomania resistance in sugar beet. Euphytica 2002, 127:383-397.
15. Biancardi E., McGrath J.M., Panella L.W., Lewellen R.T., Stevanato P. Sugar beet. Handbook of Plant Breeding (vol. 4), Tuber and Root Crops 2010, 173-219. Springer, New York. J. Bradshow (Ed.).
16. Bleykasten-Grosshans C., Guilley H., Bouzoubaa S., Richards K.E., Jonard G. Independent expression of the first two triple gene block proteins of beet necrotic yellow vein virus complements virus defective in the corresponding gene but expression of the third protein inhibits viral cell-to-cell movement. MPMI 1997, 10:240-246.
17. Bongiovanni G.C., Lanzoni L. La rizomania della bietola. Prog. Agric. 1964, 2:209-220.
18. Brumin M., Stukalov S., Haviv S., Muruganantham M., Moskovitz Y., Batuman O., Fenigstein A., Mawassi M. Post-transcriptional gene silencing and virus resistance in Nicotiana benthamiana expressing a Grapevine virus A minireplicon. Transgenic Res. 2009, 18:331-345.
19. Bucher E.C., Lohuis D., van Poppel P.M.J.A., Geerts-Dimitriadou C., Goldbach R., Prins M. Multiple virus resistance at a high frequency using a single transgene construct. J. Gen. Virol. 2006, 87:3697-3701.
20. Canova A. Appunti di patologie della barbabietola. Inform. Fitopatol. 1959, 9:390-396.
21. Chiba S., Kondo H., Miyanishi M., Andika I.B., Han C., Tamada T. The evolutionary history of Beet necrotic yellow vein virus deduced from genetic variation, geographical origin and spread, and the breaking of host resistance. MPMI 2011, 24(2):207-218.
22. Chiba S., Miyanishi M., Andica I.B., Kondo H., Tamada T. Identification of amino acids of the beet necrotic yellow vein virus p25 protein required for induction of the resistance response in leaves of Beta vulgaris plants. J. Gen. Virol. 2008, 89:1314-1323.
23. Conner A.J., Barrell P.J., Baldwin S.J., Lokerse A.S., Cooper P.A., Erasmuson A.K., Nap J.-P., Jacobs J.M.E. Intragenic vectors for gene transfer without foreign DNA. Euphytica 2007, 154:341-353.
24. De Biaggi M. Méthodes de sélection, un cas concret. Proceedings of the 50th Congress of the I.I.R.B 1987, 157-163. International Institute for Beet Research, Brussels, Belgium.
25. De Biaggi M., Stevanato P., Trebbi D., Saccomani M., Biancardi E. Sugar beet resistance to rhizomania: state of the art and perspectives. Sugar Tech 2011, 12(3-4):238-242.
26. Ding S., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
27. Ehlers U., Commandeur U., Frank R., Landsmann J., Koenig R., Burgermeister W. Cloning of the coat protein gene from beet necrotic yellow vein virus and its expression in sugar beet hairy roots. Theor. Appl. Genet. 1991, 81:777-782.
28. Fecker L.F., Koenig R., Obermeier C. Nicotiana benthamiana plants expressing beet necrotic yellow vein virus (BNYVV) coat protein-specific scFv are partially protected against the establishment of the virus in the early stages of infection and its pathogenic effects in the late stages of infection. Arch. Virol. 1997, 142:1857-1863.
29. Fuchs M., Gonsalves D. Safety of virus-resistant transgenic plants two decades after their introduction: lessons from realistic field risk assessment studies. Annu. Rev. Phytopathol. 2007, 45:173-202.
30. Fujisawa I., Sugimoto T. Transmission of Beet necrotic yellow vein virus by Polymyxa betae. Ann. Phytopathol. Soc. Jpn. 1976, 43:583-586.
31. Garcia-Arenal F., McDonald B.A. An analysis of the durability of resistance to plant viruses. Phytopathology 2003, 93(8):941-952.
32. Gidner S., Lennefors B.-L., Nilsson N.-O., Bensefelt J., Johansson E., Gyllenspetz U., Kraft T. QTL mapping of BNYVV resistance from the WB41 source in sugar beet. Genome 2005, 48:279-285.
33. Grimmer M.K., Kraft T., Francis S.A., Asher M.J.C. QTL mapping of BNYVV resistance from the WB258 source in sugar beet. Plant Breed. 2008, 127:650-652.
34. Grimmer M.K., Trybush S., Hanley S., Francis S.A., Karp A., Asher M.J.C. An anchored linkage map for sugar beet based on AFLP, SNP and RAPD markers and QTL mapping of a new source of resistance to Beet necrotic yellow vein virus. Theor. Appl. Genet. 2007, 114:1151-1160.
35. Harju V.A., Mumford R.A., Bockley A., Boonham N., Clover G.R.G., Weekes R., Henry C.M. Occurrence in the United Kingdom of beet necrotic yellow vein virus isolates which contain RNA 5. Plant Pathol. 2002, 51:811.
36. Heijbroek W., Musters P.M.S., Schoone A.H.L. Variation in pathogenicity and multiplication of Beet necrotic yellow vein virus in relation to the resistance of sugar beet cultivars. Eur. J. Plant Pathol. 1999, 105:397-405.
37. Joersbo M. Sugar beet. Biotechnology in Agriculture and Forestry, Transgenic Crops IV 2007, 355-379. Springer-Verlag, Berlin Heidelberg. E.C. Pua, M.R. Davey (Eds.).
38. J.R.C. Technical Report EUR 22102 EN, 2006. New case studies on the coexistence of GM and non-GM crops in European agriculture. JRC Technical Report Series.
39. Kallerhoff J., Pascual P., Bouzoubaa S., Tahar S.B., Perret J. Beet necrotic yellow vein virus coat protein-mediated protection in sugar beet (Beta vulgaris L.) protoplasts. Plant Cell Rep. 1990, 9:224-228.
40. Kiguchi T., Saito M., Tamada T. 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. 1996, 77:575-580.
41. Koenig R., Haeberle A.M., Commandeur U. Detection and characterization of a distinct type of beet necrotic yellow vein virus RNA 5 in a sugar beet growing area in Europe. Arch. Virol. 1997, 142:1499-1504.
42. Koenig R., Kastirr U., Holtschulte B., Deml G., Varrelmann M. Distribution of various types and p25 subtypes of Beet necrotic yellow vein virus in Germany and other European countries. Arch. Virol. 2008, 153:2139-2144.
43. Koenig R., Lennefors B.-L. Molecular analysis of European A, B and P type sources of beet necrotic yellow vein virus and detection of the rare P type in Kazakhstan. Arch. Virol. 2000, 145:1561-1570.
44. Koenig R., Loss S., Specht J., Varrelmann M., Luddecke P., Deml G. A single U/C nucleotide substitution changing alanine to valine in the beet necrotic yellow vein virus p25 protein promotes increased virus accumulation in roots of mechanically inoculated, partially resistant sugar beet seedlings. J. Gen. Virol. 2009, 90:759-763.
45. Koenig R., Luddecke P., Haeberle A.M. 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. 1995, 76:2051-2055.
46. Kruse M., Koenig R., Hoffmann A., Kaufmann A., Commandeur U., Solovyev A.G., Savenkov I., Burgermeister W. 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. 1994, 75:1835-1842.
47. Lein J.C., Asbach K., Tian Y.Y., Schulte D., Li C.Y., Koch G., Jung C., Cai D.G. Resistance gene analogues are clustered on chromosome 3 of sugar beet and cosegregate with QTL for rhizomania resistance. Genome 2007, 50:61-71.
48. Lennefors B.-L., Lindsten K., Koenig R. First record of A and B type beet necrotic yellow vein virus in sugar beets in Sweden. Eur. J. Plant Pathol. 2000, 106:199-201.
49. Lennefors B.-L., Savenkov E.I., Bensefelt J., Wremerth-Weich E., van Roggen P., Tuvesson S., Valkonen J.P.T., Gielen J. dsRNA-mediated resistance to Beet Necrotic Yellow Vein Virus infections in sugar beet (Beta vulgaris L. ssp. vulgaris). Mol. Breed. 2006, 18:313-325.
50. Lennefors B.-L., Savenkov E.I., Mukasa S.B., Valkonen J.P.T. Sequence divergence of four soil-borne sugarbeet-infecting viruses. Virus Genes 2005, 31:57-64.
51. Lewellen R.T. Performance of near-isolines of sugar beet with resistance to rhizomania from different sources. Proceedings of the 58th IIRB Congress 1995, 83-92. International Institute for Beet Research, Brussels, Belgium.
52. Lewellen R.T. Selection for resistance to rhizomania in sugar beet. Proceedings of the 5th International Congress Plant Pathology 1988, 455.
53. Lewellen R.T., Biancardi E. Breeding and performance of rhizomania resistant sugar beet. Proceedings of the 53rd Congress of the IIRB 1990, 79-87. International Institute for Beet Research, Brussels, Belgium.
54. Lewellen R.T., Skoyen I.O., Erichsen A.W. Breeding sugarbeet for resistance to rhizomania: evaluation of host-plant reactions and selection for and inheritance of resistance. Proceedings of the 50th Congress of the IIRB 1987, 139-156. International Institute for Beet Research, Brussels, Belgium.
55. Link D., Schmidlin L., Schirmer A., Klein E., Erhardt M., Geldreich A., Lemaire O., Gilmer D. Functional characterization of the Beet necrotic yellow vein virus RNA-5-encoded p26 protein: evidence for structural pathogenicity determinants. J. Gen. Virol. 2005, 86:2115-2125.
56. Liu H.Y., Lewellen R.T. Distribution and molecular characterisation of resistance breaking isolates of Beet necrotic yellow vein virus in the United States. Plant Dis. 2007, 91:847-851.
57. Luterbacher M.C., Asher M.J.C., Beyer W., Mandolino G., Scholten O.E., Frese L., Biancardi E., Stevanato P., Mechelke W., Slyvchenko O. Sources of resistance to diseases of sugar beet in related Beta germplasm. II. Soil-borne diseases. Euphytica 2005, 141:49-63.
58. Mannerlöf M., Lennefors B.-L., Tenning P. Reduced titer of BNYVV in transgenic sugar beets expressing the BNYVV coat protein. Euphytica 1996, 90:293-296.
59. Maule A.J., Caranta C., Boulton M.I. Sources of natural resistance to plant viruses: status and prospects. Mol. Plant Pathol. 2007, 8:223-231.
60. McGrann G.R.D., Grimmer M.K., Mutasa-Gottgens E.S., Stevens M. Progress towards the understanding and control of sugar beet rhizomania disease. Mol. Plant Pathol. 2009, 10:129-141.
61. Mehrvar M., Valizadeh J., Koenig R., Bragard C.G. Iranian beet necrotic yellow vein virus (BNYVV): pronounced diversity of the p25 coding region in A-type BNYVV and identification of P-type BNYVV lacking a fifth RNA species. Arch. Virol. 2009, 154:501-506.
62. Meunier A., Schmit J.F., Bragard C. Sequence analysis of Belgian BNYVV and development of a simultaneous detection of soil-borne sugar beet viruses by RT-PCR. Proceedings of the 5th Symposium of the International Working Group on Plant Viruses with Fungal Vectors 2003, 9-12. American Society of Sugar Beet Technologists, Zürich, Switzerland. C.M. Rush, U. Merz (Eds.).
63. Miyanishi M., Kusume T., Saito M., Tamada T. Evidence for three groups of sequence variants of beet necrotic yellow vein virus RNA 5. Arch. Virol. 1999, 144:879-892.
64. Napoli C., Lemieux C., Jorgensen R. Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 1990, 2:279-289.
65. Paul H., Henken B., De Bock Th.S.M., Lange W. Resistance to Polymyxa betae in Beta species of the section Procumbentes, in hybrids with B. vulgaris and in monosomic chromosome additions of B. procumbens in B. vulgaris. Plant Breed. 1992, 109:265-273.
66. Paul H., Henken B., Scholten O.E., De Bock Th.S.M., Lange W. Variation in the level of infection with Polymyxa betae and its effect on infection with beet necrotic yellow vein virus in beet accessions of the sections Beta and Corollinae. Proceedings of the 2nd Symposium of the International Working Group on Plant Viruses with Fungal Vectors 1993, 133-136.
67. Paul H.B., Henken B., Scholten O.E., Lange W. Use of zoospores of Polymyxa betae in screening beet seedlings for resistance to beet necrotic yellow vein virus. Neth. J. Plant Pathol. 1993, 99(3):151-160.
68. Pavli O.I., Kelaidi G.I., Tampakaki A.P., Skaracis G.N. The hrpZ gene of Pseudomonas syringae pv. phaseolicola enhances resistance to rhizomania disease in transgenic Nicotiana benthamiana and sugar beet. PLoS One 2011, 6(3):e17306. 10.1371/journal.pone.0017306.
69. Pavli O.I., Panopoulos N.J., Goldbach R., Skaracis G.N. BNYVV-derived dsRNA confers resistance to rhizomania disease of sugar beet as evidenced by a novel transgenic hairy root approach. Transgenic Res. 2010, 19:915-922.
70. Psph in transgenic N. benthamiana results in BNYVV-induced tissue necrosis and enhanced rhizomania resistance. Proceedings of the 5th EPSO Conference 2010, 65.
71. Pavli O.I., Skaracis G.N. Fast and efficient genetic transformation of sugar beet by Agrobacterium rhizogenes. Protoc. Netw. Nat. Protoc. 2010, 10.1038/nprot.2010.98.
72. Pavli, O.I., Prins, M., Goldbach, R., Skaracis, G.N. Efficiency of Rz1-based rhizomania resistance and molecular studies on BNYVV isolates from sugar beet cultivation in Greece. Eur. J. Plant Pathol., in press.
73. Pelsy F., Merdinoglu D. Identification and mapping of random amplified polymorphic DNA markers linked to a rhizomania resistance gene in sugar beet (Beta vulgaris L.) by bulked segregant analysis. Plant Breed. 1996, 115:371-377.
74. Pferdmenges F., Korf H., Varrelmann M. Identification of rhizomania-infected soil in Europe able to overcome Rz1 resistance in sugar beet and comparison with other resistance-breaking soils from different geographic origins. Eur. J. Plant Pathol. 2009, 124:31-43.
75. Pferdmenges F., Varrelmann M. Breaking of Beet necrotic yellow vein virus resistance in sugar beet is independent of virus and vector inoculum densities. Eur. J. Plant Pathol. 2009, 124:231-245.
76. Powell-Abel P., Nelson R.S., De B., Hoffmann N., Rogen S.G., Fraley R.T., Beachy R.N. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 1986, 232:738-743.
77. Prins M., Laimer M., Noris E., Schubert J., Wassenegger M., Tepfer M. Strategies for antiviral resistance in transgenic plants. Mol. Plant Pathol. 2008, 9(1):73-83.
78. Putz C., Merdinoglu D., Lemaire O., Stocky G., Valentin P., Wiedemann S. Beet necrotic yellow vein virus, causal agent of sugar beet rhizomania. Disease profile. Rev. Plant Pathol. 1990, 69:247-253.
79. Richard-Molard M.S. Rhizomania: a world-wide danger to sugar beet. Span 1985, 28:92-94.
80. Rommens C.M., Haring M.A., Swords K., Davies H.V., Belknap W.R. The intragenic approach as a new extension to traditional plant breeding. Trends Plant Sci. 2007, 12(9):1360-1385.
81. Roossinck M.J. Mechanisms of plant virus evolution. Annu. Rev. Phytopathol. 1997, 35:191-209.
82. Rush C.M. Ecology and epidemiology of Benyviruses and plasmodiophorid vectors. Annu. Rev. Phytopathol. 2003, 41:567-592.
83. Sanford J.C., Johnston S.A. The concept of pathogen derived resistance. J. Theor. Biol. 1985, 113:395-405.
84. Schirmer A., Link D., Cognat V., Moury B., Beuve M., Meunier A., Bragard C., Gilmer D., Lemaire O. Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. J. Gen. Virol. 2005, 86:2897-2911.
85. Scholten O.E., De Bock T.S.M., Klein-Lankhorst R.M., Lange W. Inheritance of resistance to beet necrotic yellow vein virus in Beta vulgaris, conferred by a second gene for resistance. Theor. Appl. Genet. 1999, 99:740-746.
86. Scholten O.E., Jansen R.C., Keizer L.C.P., De Bock T.S.M., Lange W. Major genes for resistance to beet necrotic yellow vein virus (BNYVV) in Beta vulgaris. Euphytica 1996, 91:331-339.
87. Scholten O.E., Klein-Lankhorst R.M., Esselink D.G., de Boch T.S.M., Lange W. Identification and mapping of random amplified polymorphic DNA (RAPD) markers linked to resistance against beet necrotic yellow vein virus (BNYVV) in Beta accessions. Theor. Appl. Genet. 1997, 94:123-130.
88. Scholten O.E., Lange W. Breeding for resistance to rhizomania in sugar beet: a review. Euphytica 2000, 112:219-231.
89. Schouten H.J., Jacobsen E. Cisgenesis and intragenesis, sisters in innovative plant breeding. Trends Plant Sci. 2008, 13:260-261.
90. Shao M., Wang J., Dean R.A., Lin Y., Gao X., Hu S. Expression of a harpin-encoding gene in rice confers durable nonspecific resistance to Magnaporthe grisea. Plant Biotechnol. J. 2008, 6:73-81.
91. Skaracis G.N. Molecular biology and biotechnology, genetic engineering. Genetics and Breeding of Sugar Beet 2005, 255-268. Science Publishers, Inc., Enfield, NH, USA. E. Biancardi, L.G. Campbell, G.N. Skaracis, M. De Biaggi (Eds.).
92. Skaracis G.N., Biancardi E. Breeding for cercospora resistance in sugar beet. Cercospora beticola Sacc. Biology, Agronomic Influence and Control Measures in Sugar Beet. Advances in Sugar Beet Research 2000, vol. 2. IIRB, Bruxelles, Belgium, pp. 177-195.
93. Sohi H., Maleki M. Evidence for presence of types A and B of beet necrotic yellow vein virus (BNYVV) in Iran. Virus Genes 2004, 29:353-358.
94. Steddom K., Heidel G., Jones D., Rush C.M. Remote detection of rhizomania in sugar beets. Phytopathology 2003, 93:720-726.
95. Suarez M.B., Grondona I., Garcia-Benavides P., Monte E., Garcia-Acha I. Characterization of beet necrotic yellow vein virus furovirus from Spanish sugar beets. J. Int. Microbiol. 1999, 2:87-92.
96. Tamada T. Beet necrotic yellow vein virus. CMI/AAB Description of Plant Viruses 2002, vol. 391. Association of Applied Biologists, Wellesbourne, UK.
97. Tamada T. Benyviruses. Encyclopedia of Virology 1999, 154-160. Academic Press, London, UK. 2nd edn. R.G. Webster, A. Granoff (Eds.).
98. Tamada T. Beet necrotic yellow vein virus. CMI/AAB Descriptions of Plant Viruses 1975, Association of Applied Biologists, Wellesbourne, UK, p. 144.
99. Tamada T., Baba T. Beet necrotic yellow vein virus from rhizomania-affected sugar beet in Japan. Ann. Phytopathol. Soc. Jpn. 1973, 39:325-332.
100. Tamada T., Kusume T., Uchino H., Kiguchi T., Saito M. Evidence that beet necrotic yellow vein virus RNA-5 is involved in symptom development of sugar beet roots. Proceedings of the 3rd Symposium of the International Working Group on Plant Viruses with Fungal Vectors 1996, 49-52. American Society of Sugar Beet Technologists, Dundee, UK. J.L. Sherwood, C.M. Rush (Eds.).
101. Tamada T., Shirako Y., Abe H., Saito M., Kiguchi T., Harada T. Production and pathogenicity of isolates of beet necrotic yellow vein virus with different numbers of RNA components. J. Gen. Virol. 1989, 70:3399-3409.
102. Till B.J., Comai L., Henikoff S. Tilling and Ecotilling for crop improvement. Genomics-Assisted Crop Improvement, Vol. 1: Genomics Approaches and Platforms 2007, 333-349. Springer. R.K. Varshney, R. Tuberosa (Eds.).
103. Torrance L., Mayo M.A. Proposed re-classification of Furoviruses. Arch. Virol. 1997, 142:435-439.
104. van der Krol A.R., Mur L.A., Beld M., Mol J.N., Stuitje A.R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 1990, 2:291-299.
105. Ward L., Koenig R., Budge G., Garrido C., McGrath C., Stubbley H., Boonham N. Occurrence of two different types of RNA-5-containing Beet necrotic yellow vein virus in the UK. Arch. Virol. 2007, 152(1):59-73.
106. Whitney E.D. Identification, distribution, and testing for resistance to rhizomania in Beta maritima. Plant Dis. 1989, 73:287-290.
107. Wozniak C.A. Transgenic sugar beet: progress and development. Appl. Plant Biotechnol. 1999, 10:301-324.