Maize streak virus: An old and complex 'emerging' pathogen

Molecular Plant Pathology

Volumn 11, Issue 1, 2010, Pages 1-12

  Shepherd, Dionne N ^a   Martin, Darren P ^a   Van Der Walt, Eric ^a,b   Dent, Kyle ^a,c   Varsani, Arvind ^a,d   Rybicki, Edward P ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Kapa Biosystems Research   (South Africa)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; EVOLUTION; GENETIC VARIABILITY; GENETICS; MAIZE; MAIZE STREAK VIRUS; PATHOGENICITY; VIROLOGY; VIRUS GENE;

EVOLUTION; GENES, VIRAL; GENETIC VARIATION; MAIZE STREAK VIRUS; ZEA MAYS;

AVENA FATUA; CICADULINA; CICADULINA MBILA; CICADULINA STOREYI; GEMINIVIRIDAE; HORDEUM; MAIZE STREAK VIRUS; MASTREVIRUS; MIRIDAE; POACEAE; SECALE CEREALE; TRITICUM AESTIVUM; ZEA MAYS;

EID: 73649149060     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00568.x     Document Type: Article

References (110)

1. Ammar, E.-D., Gargani, D., Lett, J.M. Peterschmitt, M. (2009) Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila. Arch. Virol. 154, 255 262.
2. van Antwerpen, T., McFarlane, S.S., Buchanan, G.F., Shepherd, D.N., Martin, D.P., Rybicki, E.P. Varsani, A. (2008) First report of maize streak virus infection of sugarcane in South Africa. Plant Dis. 92, 982.
3. Asanzi, M.C., Bosque-Pérez, N.A., Nault, L.R., Gordon, D.T. Thottappilly, G. (1995) Biology of Cicadulina species (Homoptera: Cicadellidae) and transmission of maize streak virus. Afr. Entomol. 3, 173 179.
4. Autrey, L.J.C. Ricaud, C. (1983) The comparative epidemiology of two diseases of maize caused by leafhopper-borne viruses in Mauritius. In : Plant Virus Epidemiology (Plumb, R.T. Thresh, J.M. eds), pp. 277 285. Oxford : Blackwell.
5. Bock, K.R. (1982) Geminivirus diseases in tropical crops. Plant Dis. 66, 266 270.
6. Bock, K.R., Guthrie, E.J. Woods, R.D. (1974) Purification of maize streak virus and its relationship to viruses associated with streak diseases of sugarcane and Panicum maximum. Ann. Appl. Biol. 77, 289 296.
7. Bosque-Pérez, N.A. (2000) Eight decades of maize streak virus research. Virus Res. 71, 107 121.
8. Boulton, M.I. (2002) Functions and interactions of mastrevirus gene products. Physiol. Mol. Plant Pathol. 60, 243 255.
9. Boulton, M.I. Markham, P.G. (1986) The use of squash-blotting to detect plant pathogens in insect vectors. In : Developments in Applied Biology 1: Developments and Applications in Virus Testing (Jones, R.A.C. Torrance, L. eds), pp. 55 69. Wellesbourne, Warwicks., UK : Association of Applied Biologists.
10. Boulton, M.I., Pallaghy, C.K., Chatani, M., Macfarlane, S. Davies, J.W. (1993) Replication of maize streak virus mutants in maize protoplasts - evidence for a movement protein. Virology, 192, 85 93.
11. Boulton, M.I., Steinkellner, H., Donson, J., Markham, P.G., King, D.I. Davies, J.W. (1989) Mutational analysis of the virion-sense genes of maize streak virus. J. Gen. Virol. 70, 2309 2323.
12. Briddon, R.W., Lunness, P., Chamberlin, L.C. Markham, P.G. (1994) Analysis of the genetic variability of maize streak virus. Virus Genes, 9, 93 100.
13. Briddon, R.W., Pinner, M.S., Stanley, J. Markham, P.G. (1990) Geminivirus coat protein gene replacement alters insect specificity. Virology, 177, 85 94.
14. Dabrowski, Z.T. (1987) Cicadulina ghaurii (Hem., Euscelidae): distribution, biology and maize streak virus (MSV) transmission. J. Appl. Entomol. 103, 489 496.
15. Dabrowski, Z.T., Nwilene, F. Kumar, R. (1991) First regular observations on leafhoppers, Cicadulina spp., vectors of maize streak virus (MSV) in southeastern Nigeria. Insect Sci. Appl. 12, 249 261.
16. Dabrowski, Z.T., Wilson, M.R. Nault, L.R. (1987). Comparative studies of Cicadulina leafhoppers in West Africa. In : Proceedings of 2nd International Workshop on Leafhoppers and Planthoppers of Economic Importance, 28th July-1st August 1986 (Wilson, M.R. ed.), pp. 35 39. Provo, UT : Brigham Young University.
17. Damsteegt, V.D. (1983) Maize streak virus: I. Host range and vulnerability of maize germ plasm. Plant Dis. 67, 734 737.
18. Duffy, S. Holmes, E.C. (2008) Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus Tomato yellow leaf curl virus. J. Virol. 82, 957 965.
19. Efron, Y., Kim, S.K., Fajemisin, J.M., Mareck, J.H., Tang, C.Y., Dabrowski, Z.T., Rossel, H.W., Thottappilly, G. Buddenhagen, I.W. (1989) Breeding for resistance to maize streak virus: a multidisciplinary team approach. Plant Breed. 103, 1 36.
20. Fajemisin, J.M. Shoyinka, S.A. (1976) Maize streak and other maize virus disease in West Africa. In : Proceedings of the International maize virus disease colloquium and workshop (Williams, L.E., Gordon, D.T., Nault, L.R. eds pp. 52 60. Wooster USA : Ohio Agricultural Research and Development Center.
21. Fielding, W.L. (1933) Field experimental work on rotation crops. In : Empire Cotton Growing Association Progress Report 1931-1932, pp. 10 14.
22. Francki, R.I.B., Hatta, T., Boccardo, G. Randles, J.W. (1980) The composition of chloris striate mosaic virus, a geminivirus. Virology, 101, 233 241.
23. Fuller, C. (1901) Mealie variegation. In : 1st Report of the Government Entomologist, Natal, 1899-1900. Pietermaritzburg, Natal, South Africa : P. Davis & Sons, Government Printers.
24. Ge, L., Zhang, J., Zhou, X. Li, H. (2007) Genetic structure and population variability of Tomato yellow leaf curl China virus. J. Virol. 81, 5902 5907.
25. Goodman, R.M. (1977a) Infectious DNA from a whitefly transmitted virus of Phaseolus vulgaris. Nature, 266, 54.
26. Goodman, R.M. (1977b) Single-stranded DNA genome in a whitefly-transmitted plant virus. Virology, 83, 171.
27. Gutierrez, C. (1999) Geminivirus DNA replication. Cell Mol. Life Sci. 56, 313 329.
28. Harrison, B.D., Barker, H., Bock, K.R., Guthrie, E.J., Meredith, G. Atkinson, M. (1977) Plant viruses with circular single-stranded DNA. Nature, 270, 760 762.
29. Heyraud, F., Matzeit, V., Kammann, M., Schaefer, S., Schell, J. Gronenborn, B. (1993a) Identification of the initiation sequence for viral-strand DNA synthesis of wheat dwarf virus. EMBO J. 12, 4445 4452.
30. Heyraud, F., Matzeit, V., Schaefer, S., Schell, J. Gronenborn, B. (1993b) The conserved nonanucleotide motif of the geminivirus stem-loop sequence promotes replicational release of virus molecules from redundant copies. Biochimie, 75, 605 615.
31. Heyraud-Nitschke, F., Schumacher, S., Laufs, J., Schaefer, S., Schell, J. Gronenborn, B. (1995) Determination of the origin, cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res. 23, 910 916.
32. Isnard, M., Granter, M., Frutos, R., Reynaud, B. Peterschmitt, M. (1998) Quasi-species nature of the maize streak virus isolates obtained from a population used to assess maize cultivar response to infection. J. Gen. Virol. 79, 3091 3099.
33. Jeske, H., Lutgemeier, M. Preiss, W. (2001) DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J. 20, 6158 6167.
34. Jovel, J., Preiss, W. Jeske, H. (2007) Characterization of DNA intermediates of an arising geminivirus. Virus Res. 130, 63 70.
35. Kim, S.K., Efron, Y., Khadr, F.H., Fajemisin, J.M. Lee, M.H. (1987) Registration of 16 maize streak-virus resistant tropical maize parental inbred lines. Crop Sci. 27, 824 825.
36. Kloppers, F. (2005) Maize diseases: reflection on the 2004/2005 season. Available at: http://saspp.org/index2.php?option=com-content&do-pdf= 1&id=2 [accessed 6 July 2009 Traore, O. (1992) Reservoir hosts of maize streak virus (MSV) in the Sudan-Sahel zone: identification and spatio-temporal distribution. Phytoprotection, 73, 111 117.
37. Kotlizky, G., Boulton, M.I., Pitaksutheepong, C., Davies, J.W. Epel, B.L. (2000) Intracellular and intercellular movement of maize streak geminivirus V1 and V2 proteins transiently expressed as green fluorescent protein fusions. Virology, 274, 32 38.
38. Kyetere, D., Ming, R., McMullen, M., Pratt, R., Brewbaker, J., Musket, T., Pixley, K. Moon, H. (1995) Monogenic tolerance to maize streak virus maps to the short arm of chromosome 1. Maize Genet. Coop. News Lett. 69, 136 137.
39. Kyetere, D.T., Ming, R., McMullen, M.D., Pratt, R.C., Brewbaker, J. Musket, T. (1999) Genetic analysis of tolerance to maize streak virus in maize. Genome 42, 20 26.
40. Laufs, J., Schumacher, S., Geisler, N., Jupin, I. Gronenborn, B. (1995a) Identification of the nicking tyrosine of geminivirus Rep protein. FEBS Lett. 377, 258 262.
41. Laufs, J., Traut, W., Heyraud, F., Matzeit, V., Rogers, S.G., Schell, J. Gronenborn, B. (1995b) In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc. Natl. Acad. Sci. USA, 92, 3879 3883.
42. Lazarowitz, S.G., Pinder, A.J., Damsteegt, V.D. Rogers, S.G. (1989) Maize streak virus genes essential for systemic spread and symptom development. EMBO J. 8, 1023 1032.
43. Lefeuvre, P., Lett, J.M., Reynaud, B. Martin, D.P. (2007a) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog. 3, e181.
44. Lefeuvre, P., Martin, D.P., Hoareau, M., Naze, F., Delatte, H., Thierry, M., Varsani, A. Becker, N., Reynaud, B. Lett, J.M. (2007b) Begomovirus 'melting pot' in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J. Gen. Virol. 88, 3458 3468.
45. Lett, J.-M., Granier, M., Hippolyte, I., Grondin, M., Royer, M., Blanc, S., Reynaud, B. Peterschmitt, M. (2002) Spatial and temporal distribution of geminiviruses in leafhoppers of the genus Cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathology, 92, 65 74.
46. Liu, H., Boulton, M.I. Davies, J.W. (1997) Maize streak virus coat protein binds single- and double-stranded DNA in vitro. J. Gen. Virol. 78, 1265 1270.
47. Liu, H., Boulton, M.I., Oparka, K.J. Davies, J.W. (2001a) Interaction of the movement and coat proteins of Maize streak virus: implications for the transport of viral DNA. J. Gen. Virol. 82, 35 44.
48. Liu, H., Boulton, M.I., Thomas, C.L., Prior, D.A., Oparka, K.J. Davies, J.W. (1999) Maize streak virus coat protein is karyophyllic and facilitates nuclear transport of viral DNA. Mol. Plant-Microbe Interact. 12, 894 900.
49. Liu, H., Lucy, A.P., Davies, J.W. Boulton, M.I. (2001b) A single amino acid change in the coat protein of Maize streak virus abolishes systemic infection, but not interaction with viral DNA or movement protein. Mol. Plant Pathol. 2, 223 228.
50. Liu, L., Davies, J.W. Stanley, J. (1998) Mutational analysis of bean yellow dwarf virus, a geminivirus of the genus Mastrevirus that is adapted to dicotyledonous plants. J. Gen. Virol. 79, 2265 2274.
51. Lucy, A.P., Boulton, M.I., Davies, J.W. Maule, A.J. (1996) Tissue specificity of Zea mays infection by maize streak virus. Mol. Plant-Microbe Interact. 9, 22 31.
52. Magenya, O.E.V., Mueke, J. Omwega, C. (2008) Significance and transmission of maize streak virus disease in Africa and options for management: a review. Afr. J. Biotechnol. 7, 4897 4910.
53. Marchand, J.-L., Peterschmitt, M. Reynaud, B. (1994) Les viroses de la striure, du stripe et de la mosaïque sur le maïs en région tropicale. Afrique et îles de l'Océan Indien. Agric. Dev. 4, 1 16.
54. Markham, P.G., Pinner, M.S. Boulton, M.I. (1984) Dalbulus maidis and Cicadulina species as vectors of diseases in maize. Maize Virus Dis. Newsl. 1, 33 34.
55. Martin, D.P. Rybicki, E.P. (2002) Biological and genomic sequence characterization of Maize streak virus isolates from wheat. Phytopathology, 92, 81 86.
56. Martin, D.P. Shepherd, D.N. (2009) The epidemiology, economic impact and control of maize streak disease. Food Secur. In Press.
57. Martin, D.P., van der Walt, E., Posada, D. Rybicki, E.P. (2005) The evolutionary value of recombination is constrained by genome modularity. PLoS Genet. 1, e51.
58. Martin, D.P., Willment, J.A., Billharz, R., Velders, R., Odhiambo, B., Njuguna, J., James, D. Rybicki, E.P. (2001) Sequence diversity and virulence in Zea mays of Maize streak virus isolates. Virology, 288, 247 255.
59. Martin, D.P., Willment, J.A. Rybicki, E.P. (1999) Evaluation of maize streak virus pathogenicity in differentially resistant Zea mays genotypes. Phytopathology, 89, 695 700.
60. McClean, A.P.D. (1947) Some forms of streak virus occurring in maize, sugarcane and wild grasses. South African Department of Agriculture Bulletin, 265, 33pp.
61. Mesfin, T., den Hollander, J. Markham, P.G. (1995) Feeding activities of Cicadulina mbila (Hemiptera: Cicadellidae) on different host-plants. Bull. Entomol. Res. 85, 387 396.
62. Morris-Krsinich, B.A., Mullineaux, P.M., Donson, J., Boulton, M.I., Markham, P.G., Short, M.N. Davies, J.W. (1985) Bidirectional transcription of maize streak virus DNA and identification of the coat protein gene. Nucleic Acids Res. 13, 7237 7256.
63. Njuguna, J.A.M., Kendera, J.G., Muriithi, L.M.M., Songa, S. Othiambo, R.B. (1990) Overview of maize diseases in Kenya. In : Maize Review Workshop in Kenya, Kakamega, Kenya, pp 45 51.
64. Oluwafemi, S., Jackai, L.E.N. Alegbejo, M.D. (2007) Comparison of transmission abilities of four Cicadulina species vectors of maize streak virus from Nigeria. Entomol. Exp. Appl. 124, 235 239.
65. Oluwafemi, S., Varsani, A., Monjane, A.L., Shepherd, D.N., Owor, B., Rybicki, E.P. Martin, D.P. (2008) A new African streak virus species from Nigeria. Arch. Virol. 153, 1407 1410.
66. Owor, B., Martin, D.P., Shepherd, D.N., Edema, R., Monjane, A.L., Rybicki, E.P., Thomson, J.A. Varsani, A. (2007) Genetic analysis of maize streak virus isolates from Uganda reveals widespread distribution of a recombinant variant. J. Gen. Virol. 88, 3154 3165.
67. Padidam, M., Sawyer, S. Fauquet, C.M. (1999) Possible emergence of new geminiviruses by frequent recombination. Virology, 265, 218 225.
68. Pernet, A., Hoisington, D.A., Dintinger, J., Jewell, D.C., Jiang, C., Khairallah, M.M., Letourmy, P., Marchand, J.-L., Glaszmann, J.-C. González de Leon, D. (1999a) Genetic mapping of maize streak virus resistance from the Mascarene source. II. Resistance in line CIRAD390 and stability across germplasm. Theor. Appl. Genet. 99, 540 553. (Pubitemid 29432505)
69. Pernet, A., Hoisington, D.A., Franco, J., Isnard, M., Jewell, D.C., Jiang, C., Marchand, J.-L., Reynaud, B., Glaszmann, J.-C. González de Leon, D. (1999b) Genetic mapping of maize streak virus resistance from the Mascarene source. I. Resistance in line D211 and stability against different virus clones. Theor. Appl. Genet. 99, 524 539. (Pubitemid 29432504)
70. Peterschmitt, M., Quiot, J.B. Reynaud, B. (1992) Detection of maize streak virus antigens over time in different parts of maize plants of a sensitive and a so-called tolerant cultivar by ELISA. Ann. Appl. Biol. 121, 641 653.
71. Pinner, M.S., Medina, V., Plaskitt, K.A. Markham, P.G. (1993) Viral inclusions in monocotyledons infected by maize streak and related geminiviruses. Plant Pathol. 42, 75 87.
72. Preiss, W. Jeske, H. (2003) Multitasking in replication is common among geminiviruses. J. Virol. 77, 2972 2980.
73. Reynaud, B. Peterschmitt, M. (1992) A study of the mode of transmission of MSV by Cicadulina mbila using an enzyme-linked immunosorbent assay. Ann. Appl. Biol. 121, 85 94.
74. Rodier, A., Assié, J., Marchand, J.-L. Hervé, Y. (1995) Breeding maize lines for complete and partial resistance to maize streak virus (MSV). Euphytica, 81, 57 70.
75. Rose, D.J.W. (1978) Epidemiology of maize streak disease. Ann. Rev. Entomol. 23, 250 282.
76. Rossel, H.W. Thottappilly, G. (1985) In : Virus Diseases of Important Food Crops in Tropical Africa, pp. 61. Ibadan : International Institute of Tropical Agriculture (IITA).
77. Sanford, J.C. Johnson, S.A. (1985) The concept of parasite-derived resistance: deriving resistance genes from the parasite's own genome. J. Theor. Biol. 115, 395 405.
78. Saunders, K., Lucy, A. Stanley, J. (1991) DNA forms of the geminivirus African cassava mosaic virus consistent with a rolling circle mechanism of replication. Nucleic Acids Res. 19, 2325 2330.
79. Saunders, K., Lucy, A. Stanley, J. (1992) RNA-primed complementary-sense DNA synthesis of the geminivirus African cassava mosaic virus. Nucleic Acids Res. 20, 6311 6315.
80. Schalk, H.J., Matzeit, V., Schiller, B., Schell, J. Gronenborn, B. (1989) Wheat dwarf virus, a geminivirus of graminaceous plants needs splicing for replication. EMBO J. 8, 359 364.
81. Schnippenkoetter, W.H., Martin, D.P., Hughes, F.L., Fyvie, M., Willment, J.A., James, D., von Wechmar, M.B. Rybicki, E.P. (2001a) The relative infectivities and genomic characterisation of three distinct mastreviruses from South Africa. Arch. Virol. 146, 1075 1088.
82. Schnippenkoetter, W.H., Martin, D.P., Willment, J.A. Rybicki, E.P. (2001b) Forced recombination between distinct strains of Maize streak virus. J. Gen. Virol. 82, 3081 3090.
83. Shepherd, D.N., Mangwende, T., Martin, D.P., Bezuidenhout, M., Kloppers, F.J., Carolissen, C.H., Monjane, A.L., Rybicki, E.P. Thomson, J.A. (2007) Maize streak virus-resistant transgenic maize: a first for Africa. Plant Biotechnol. J. 5, 759 767.
84. Shepherd, D.N., Martin, D.P., McGivern, D.R., Boulton, M.I., Thomson, J.A. Rybicki, E.P. (2005) A three-nucleotide mutation altering the Maize streak virus Rep pRBR-interaction motif reduces symptom severity in maize and partially reverts at high frequency without restoring pRBR-Rep binding. J. Gen. Virol. 86, 803 813.
85. Shepherd, D.N., Martin, D.P. Thomson, J.A. (2009) Strategies for developing crops resistant to geminiviruses. Plant Sci. 176, 1 11.
86. Shepherd, D.N., Varsani, A., Windram, O., Lefeuvre, P., Monjane, A.L., Owor, B. Martin, D.P. (2008) Novel sugarcane streak virus and sugarcane streak Reunion virus-like mastrevirus isolates from Southern Africa and La Reunion. Arch. Virol. 153, 605 609.
87. Soto, P.E., Buddenhagen, I.W. Asnani, V.L. (1982) Development of streak virus-resistant maize populations through improved challenge and selection methods. Ann. Appl. Biol. 100, 539 546.
88. Stanley, J. (1995) Analysis of African cassava mosaic virus recombinants suggests strand nicking occurs within the conserved nonanucleotide motif during the initiation of rolling circle DNA replication. Virology, 206, 707 712.
89. Stanley, J., Boulton, M.I. Davies, J.W. (1999) Geminiviridae. in : Embryonic encyclopedia of Life Sciences. Nature Publishing group, London. http://www.els.net/elsonline/html/
90. Stenger, D.C., Revington, G.N., Stevenson, M.C. Bisaro, D.M. (1991) Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc. Natl. Acad. Sci. USA, 88, 8029 8033.
91. Storey, H.H. (1924) The transmission of a new plant virus disease by insects. Nature, 144, 245.
92. Storey, H.H. (1925) The transmission of streak disease of maize by the leafhopper Balclutha mbila Naudé. Ann. Appl. Biol. 12, 422 439.
93. Storey, H.H. (1928) Transmission of maize streak disease. Ann. Appl. Biol. 15, 1 25.
94. Storey, H.H. (1931) The inheritance by a leafhopper of the ability to transmit a plant virus. Nature, 127, 928.
95. Storey, H.H. (1932) The inheritance by an insect vector of the ability to transmit a plant virus. Proc. R. Soc. Lond., B, 112, 46 60.
96. Storey, H.H. (1933) Investigations of the mechanism of the transmission of plant viruses by insect vectors. I. Proc. R. Soc. Lond., B, 113, 463 485.
97. Storey, H.H. (1938) Investigation of the mechanism of the transmission of plant viruses by insect vectors. II. The part played by puncture in transmission. Proc. R. Soc. Lond., B, 125, 455 477.
98. Storey, H.H. (1939) Investigation of the mechanism of the transmission of plant viruses by insect vectors. III. The insect's saliva. Proc. R. Soc. Lond., B, 127, 526 543.
99. Storey, H.H. McClean, A.P.D. (1930) The transmission of streak disease between maize, sugarcane and wild grasses. Ann. Appl. Biol. 17, 691 719.
100. Vanderschuren, H., Stupak, M., Futterer, J., Gruissem, W. Zhang, P. (2007) Engineering resistance to geminiviruses - review and perspectives. Plant Biotechnol. J. 5, 207 220.
101. Varsani, A., Oluwafemi, S., Windram, O.P., Shepherd, D.N., Monjane, A.L., Owor, B.E., Rybicki, E.P., Lefeuvre, P. Martin, D.P. (2008b) Panicum streak virus diversity is similar to that observed for Maize streak virus. Arch. Virol. 153, 601 604.
102. Varsani, A., Shepherd, D.N., Monjane, A.L., Owor, B.E., Erdmann, J.B., Rybicki, E.P., Peterschmitt, M., Briddon, R.W., Markham, P.G., Oluwafemi, S., Windram, O.P., Lefeuvre, P., Lett, J.-M. Martin, D.P. (2008a) Recombination, decreased host specificity and increased mobility may have driven the emergence of Maize streak virus as an agricultural pathogen. J. Gen. Virol. 89, 2063 2074.
103. van der Walt, E., Martin, D.P., Varsani, A., Polston, J.E. Rybicki, E.P. (2008a) Experimental observations of rapid Maize streak virus evolution reveal a strand-specific nucleotide substitution bias. Virol. J. 5, 104.
104. van der Walt, E., Palmer, K., Martin, D.P. Rybicki, E.P. (2008b) Viable chimaeric viruses confirm the biological importance of sequence specific maize streak virus movement protein and coat protein interactions. Virol. J. 5, 61.
105. van der Walt, E., Rybicki, E.P., Varsani, A., Polston, J.E., Billharz, R., Donaldson, L., Monjane, A.L. Martin, D.P. (2009) Rapid host adaptation by extensive recombination. J. Gen. Virol. 90, 734 746.
106. Wambugu, F. Wafula, J. (2000) Advances in maize streak virus disease research in Eastern and Southern Africa. In : Workshop Report, 15-17 September, 1999, KARI and ISAAA Africa Center, ISAAA Brief No 16. Ithaca, NY : International Service for the Acquisition of Agri-Biotech Applications.
107. Welz, H.G., Schechert, A., Pernet, A., Pixley, K.V. Geiger, H.H. (1998) A gene for resistance to the maize streak virus in the African CIMMYT maize inbred line CML 202. Mol. Breed. 4, 147 154.
108. Willment, J.A., Martin, D.P., Palmer, K.E., Schnippenkoetter, W.H., Shepherd, D.N. Rybicki, E.P. (2007) Identification of long intergenic region sequences involved in Maize streak virus replication. J. Gen. Virol. 88, 1831 1841.
109. Willment, J.A., Martin, D.P. Rybicki, E.P. (2001) Analysis of the diversity of African streak mastreviruses using PCR-generated RFLPs and partial sequence data. J. Virol. Methods, 93, 75 87.
110. Willment, J.A., Martin, D.P., Van der Walt, E. Rybicki, E.P. (2002) Biological and genomic sequence characterization of Maize streak virus isolates from wheat. Phytopathology, 92, 81 86.