Recombination and selection pressure in the ipomovirus sweet potato mild mottle virus (Potyviridae) in wild species and cultivated sweetpotato in the centre of evolution in East Africa

Journal of General Virology

Volumn 91, Issue 4, 2010, Pages 1092-1108

  Tugume, Arthur K ^a,b   Mukasa, Settumba B ^b   Kalkkinen, Nisse ^c   Valkonen, Jari P T ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b MAKERERE UNIVERSITY   (Uganda)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; COAT PROTEIN; PROTEINASE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ADAPTATION; AFRICA; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONVOLVULACEAE; DNA FINGERPRINTING; ECOLOGY; EVOLUTION; GENOME; GENUS; NATURAL HOST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POTYVIRUS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SPECIES; SWEET POTATO; SWEET POTATO MILD MOTTLE VIRUS; UGANDA; VIRUS DETECTION; VIRUS ISOLATION; WESTERN BLOTTING; WILD PLANT; WILD SPECIES;

AFRICA; AMINO ACID SEQUENCE; BASE SEQUENCE; CAPSID PROTEINS; EVOLUTION, MOLECULAR; IPOMOEA BATATAS; MOLECULAR SEQUENCE DATA; POTYVIRIDAE; RECOMBINATION, GENETIC; SELECTION, GENETIC;

CONVOLVULACEAE; IPOMOEA BATATAS; IPOMOVIRUS; POTYVIRIDAE; SWEET POTATO MILD MOTTLE VIRUS;

EID: 77949536594     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.016089-0     Document Type: Article

References (90)

1. Adams, M. J., Antoniw, J. F. & Beaudoin, F. (2005a). Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6, 471-487.
2. Adams, M. J., Antoniw, J. F. & Fauquet, C. M. (2005b). Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150, 459-479.
3. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H. & Vance, V. B. (1998). A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95, 13079-13084.
4. Anisimova, M., Nielsen, R. & Yang, Z. (2003). Effect of recombination on the accuracy of the likelihood methods for detecting positive selection at amino acid sites. Genetics 164, 1229-1236.
5. Ateka, E. M., Njeru, R. W., Kibaru, A. G., Kimenju, J. W., Barg, E., Gibson, R. W. & Vetten, H. J. (2004). Identification and distribution of viruses infecting sweetpotato in Kenya. Ann Appl Biol 144, 371-379.
6. Atreya, P. L., Lopez-Moya, J. J., Chu, M., Atreya, C. D. & Pirone, T. P. (1995). Mutational analysis of the coat protein N-terminal amino acid involved in potyvirus transmission by aphids. J Gen Virol 76, 265-270.
7. Blanc, S., Ammar, E. D., Garcia-Lampasona, S., Dolja, V. V., Llave, C., Baker, J. & Pirone, T. P. (1998). Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 79, 3119-3122.
8. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P. & Ziegler-Graff, V. (2007). The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr Biol 17, 1615-1621.
9. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W. & Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739-6746.
10. Bruen, T. C., Philippe, H. & Bryant, D. (2006). A simple test for detecting the presence of recombination. Genetics 172, 2665-2681.
11. Brunt, A. A., Crabtree, K., Dallwitz, M. J., Gibbs, A. J. & Watson, L. (1996). Viruses of Plants. Descriptions and Lists from VIDE Database. Wallingford, UK: CAB International.
12. Bryant, D. & Moulton, V. (2004). Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21, 255-265.
13. Colinet, D., Kummert, J. & Lepoivre, P. (1998). The nucleotide sequence and genome organization of the whitefly transmitted Sweetpotato mild mottle virus: a close relationship with members of the family Potyviridae. Virus Res 53, 187-196.
14. Driessen, H. P. C., de Jong, W. W., Tesser, G. I. & Bloemendal, H. (1985). The mechanism of N-terminal acetylation of proteins. CRC Crit Rev Biochem 18, 281-325.
15. Elena, S. F. & Sanjuán, R. (2007). Virus evolution: insights from an experimental approach. Annu Rev Ecol Evol Syst 38, 27-52.
16. Elena, S. F., Agudelo-Romero, P., Carrasco, P., Codoñer, F. M., Martín, S., Torres-Barcel, C. & Sanjuán, R. (2008). Experimental evolution of plant RNA viruses. Heredity 100, 478-483.
17. El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M.-A., Jacobsen, S. E., Cooke, R. & Lagrange, T. (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21, 2539-2544.
18. Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A. (2005). Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. San Diego, CA: Elsevier Academic Press.
19. Flasinski, S. & Cassidy, B. G. (1998). Potyvirus aphid transmission requires helper component and homologous coat protein for maximum efficiency. Arch Virol 143, 2159-2172.
20. Fribourg, C. E. & Nakashima, J. (1984). Characterization of a new potyvirus from potato. Phytopathology 74, 1363-1369.
21. García-Arenal, F., Fraile, A. & Malpica, J. M. (2001). Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39, 157-186.
22. Gibb, K. S. & Padovan, A. C. (1993). Detection of Sweetpotato feathery mottle potyvirus in Sweetpotato grown in northern Australia using an efficient and simple assay. Int J Pest Manag 39, 223-228.
23. Gibbs, A. & Mackenzie, A. (1997). A primer pair for amplifying part of the genome of all potyvirids by RT-PCR. J Virol Methods 63, 9-16.
24. Giner, A., García-Chapa, M., Lakatos, L., Burgyan, J. & López-Moya, J. J. (2008). Involvement of P1 and HCPro proteins of Sweetpotato mild mottle ipomovirus (SPMMV) in suppression of gene silencing. In Genetic control of plant pathogenic viruses and their vectors: towards new resistance strategies, book of abstracts, P3-4, p. 90., 23-27 November 2008. Puerto de Santa Maria, Spain: ResistVir. http://www. resistvir-db.org/docs/ conference-2008/Book-of-Abstracts-IC-Cadiz- Nov-2008.pdf
25. Glasa, M., Marie-Jeanne, V., Moury, B., Kúdela, O. & Quiot, J.-B. (2002). Molecular variability of the P3-6K1 genomic region among geographically and biologically distinct isolates of Plum pox virus. Arch Virol 147, 563-575.
26. Govier, D. A. & Kassanis, B. (1974). Evidence that a component other than the virus particle is needed for aphid transmission of potato virus Y. Virology 57, 285-286.
27. Hollings, M., Stone, O. M. & Bock, K. R. (1976). Purification and properties of Sweetpotato mild mottle, a whitefly born virus from sweetpotato (Ipomoea batatas) in East Africa. Ann Appl Biol 82, 511-528.
28. Janssen, D., Martín, G., Velasco, L., Gmez, P., Segundo, E., Ruiz, L. & Cuadrado, I. M. (2005). Absence of a coding region for the helper component-proteinase in the genome of Cucumber vein yellowing virus, a whitefly-transmitted member of the Potyviridae. Arch Virol 150, 1439-1447.
29. Kassanis, B. & Govier, D. A. (1971). The role of the helper virus in aphid transmission of potato aucuba mosaic virus and potato virus C. J Gen Virol 13, 221-228.
30. Kasschau, K. D. & Carrington, J. C. (1998). A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95, 461-470.
31. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111-120.
32. Lefeuvre, P., Lett, J.-M., Reynaud, B. & Martin, D. P. (2007). Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3, e181.
33. Li, W., Hilf, M. E., Webb, S. E., Baker, C. A. & Adkins, S. (2008). Presence of P1b and absence of HC-Pro in Squash vein yellowing virus suggests a general feature of genus Ipomovirus in the family Potyviridae. Virus Res 135, 213-219.
34. Lian, S. L., Li, S., Abadal, G. X., Pauley, B. A., Fritzler, M. J. & Chan, E. K. L. (2009). The C-terminal half of human Ago2 binds to multiple GW-rich regions of GW182 and requires GW182 to mediate silencing. RNA 15, 804-813.
35. Librado, P. & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
36. Loebenstein, G., Fuentes, S., Cohen, J. & Salazar, L. F. (2003). Sweetpotato. In Viruses and Virus-Like Diseases of Major Crops in Developing Countries, pp. 223-248. Edited by G. Loebenstein & G. Thottapilly. Dordrecht, the Netherlands: Kluwer Academic.
37. Lopéz-Moya, J. J., Wang, R. Y. & Pirone, T. P. (1999). Context of the coat protein DAG motif affects potyvirus transmissibility by aphids. J Gen Virol 80, 3281-3288.
38. Malpica, J. M., Fraile, A., Moreno, I., Obies, C. I., Drake, J. W. & Garcia-Arenal, F. (2002). The rate and character of spontaneous mutations in an RNA virus. Genetics 162, 1505-1511.
39. Martin, D. P., Williamson, C. & Posada, D. (2005a). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260-262.
40. Martin, D. P., Van Der Walt, E., Posada, D. & Rybicki, E. P. (2005b). The evolutionary value of recombination is constrained by genome modularity. PLoS Genet 1, e51.
41. Matsudaira, P. (1987). Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem 262, 10035-10038.
42. Mbanzibwa, D. R., Tian, Y., Mukasa, S. B. & Valkonen, J. P. T. (2009a). Cassava brown streak virus encodes a putative Maf/HAM1 pyrophosphatase implicated in reduction of mutations and a P1 proteinase that suppresses RNA silencing but contains no HC-Pro. J Virol 83, 6934-6940.
43. Mbanzibwa, D. R., Tian, Y. P., Tugume, A. K., Mukasa, S. B., Tairo, F., Kyamanywa, S., Kullaya, A. & Valkonen, J. P. T. (2009b). Genetically distinct strains of Cassava brown streak virus in the Lake Victoria basin and the Indian Ocean coastal area of East Africa. Arch Virol 154, 353-359.
44. Moury, B., Morel, C., Johansen, E. & Jacquemond, M. (2002). Evidence for diversifying selection in Potato virus Y and in the coat protein of other potyviruses. J Gen Virol 83, 2563-2573.
45. Mukasa, S. B., Rubaihayo, P. R. & Valkonen, J. P. T. (2003a). Incidence of viruses and virus-like diseases of Sweetpotato in Uganda. Plant Dis 87, 329-335.
46. Mukasa, S. B., Rubaihayo, P. R. & Valkonen, J. P. T. (2003b). Sequence variability within the 3′-proximal part of the Sweetpotato mild mottle virus genome. Arch Virol 148, 487-496.
47. Mukasa, S. B., Rubaihayo, P. R. & Valkonen, J. P. T. (2006). Interactions between a crinivirus, an ipomovirus and a potyvirus in coinfected sweetpotato plants. Plant Pathol 55, 458-467.
48. Njeru, R. W., Bagabe, M. C., Nkezabahizi, D., Kayiranga, D., Kajuga, J., Butare, L. & Ndirigue, J. (2008). Viruses infecting Sweetpotato in Rwanda: occurrence and distribution. Ann Appl Biol 153, 215-221.
49. Ogawa, T., Tomitaka, Y., Nakagawa, A. & Ohshima, K. (2008). Genetic structure of a population of Potato virus Y inducing potato tuber necrotic ringspot disease in Japan; comparison with North American and European populations. Virus Res 131, 199-212.
50. Oh, C.-S. & Carrington, J. C. (1989). Identification of essential residues in potyvirus proteinase HC-Pro by site-directed mutagenesis. Virology 173, 692-699.
51. Ohshima, K., Tomitaka, Y., Wood, J. T., Minematsu, Y., Kajiyama, H., Tominura, K. & Gibbs, A. J. (2007). Patterns of recombination in Turnip mosaic virus genomic sequences indicate hotspots of recombination. J Gen Virol 88, 298-315.
52. Peng, Y. H., 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, 897-904.
53. Posada, D. (2002). Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19, 708-717.
54. Posada, D. & Crandall, K. A. (2002). The effect of recombination on the accuracy of phlogenetic estimation. J Mol Evol 54, 396-402.
55. Rajamäki, M.-L., Mäki-Valkama, T., Mäkinen, K. & Valkonen, J. P. T. (2004). Infection with potyviruses. In Plant-Pathogen Interactions, pp. 68-91. Edited by N. J. Talbot. Oxford, UK: Blackwell.
56. Rajamäki, M.-L., Kelloniemi, J., Alminaite, A., Kekarainen, T., Rabenstein, F. & Valkonen, J. P. T. (2005). A novel insertion site inside the potyvirus P1 cistron allows expression of heterologous proteins and suggests some P1 functions. Virology 342, 88-101.
57. Rännäli, M., Czekaj, V., Jones, R. A. C., Fletcher, J. D., Mu, L., Davis, R. & Valkonen, J. P. T. (2009). Molecular characterization of Sweetpotato feathery mottle virus (SPFMV) isolates from Easter Island, French Polynesia, New Zealand and Southern Africa. Plant Dis 93, 933-939.
58. Sáenz, P., Salvador, B., Simón-Mateo, C., Kasschau, K. D., Carrington, J. C. & García, J. A. (2002). Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J Virol 76, 1922-1931.
59. Saitou, N. & Nei, M. (1987). The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
60. Sako, N. & Ogata, K. (1981). Different helper factors associated with aphid transmission of some potyviruses. Virology 112, 762-765.
61. Salvador, B., Saénz, P., Yangüez, E., Quiot, J. B., Quiot, L., Delgadillo, M. O., García, J. A. & Simón-Mateo, C. (2008a). Hostspecific effect of P1 exchange between two potyviruses. Mol Plant Pathol 9, 147-155.
62. Salvador, B., Delgadillo, M. O., Sáenz, P., Garcia, J. A. & Simón-Mateo, C. (2008b). Identification of Plum pox virus pathogenicity determinants in herbaceous and woody hosts. Mol Plant Microbe Interact 21, 20-29.
63. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
64. Scotto-Lavino, E., Du, G. & Frohman, M. A. (2006). 5′ end cDNA amplification using classic RACE. Nat Protoc 6, 2555-2562.
65. Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. (1996). Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68, 850-858.
66. Shi, Y., Chen, J., Hong, X., Chen, J. & Adams, M. J. (2007). A potyvirus P1 protein interacts with the Rieske Fe/S protein of its host. Mol Plant Pathol 8, 785-790.
67. Stenger, D. C., French, R. & Gildow, F. E. (2005). Complete deletion of Wheat streak mosaic virus HC-Pro: a null mutant is viable for systemic infection. J Virol 79, 12077-12080.
68. Stenger, D. C., Young, B. A., Qu, F., Morris, T. J. & French, R. (2007). Wheat streak mosaic virus lacking helper component-proteinase is competent to produce disease synergism in double infections with Maize chlorotic mottle virus. Phytopathology 97, 1213-1221.
69. Tairo, F., Kullaya, A. & Valkonen, J. P. T. (2004). Incidence of viruses infecting sweetpotato in Tanzania. Plant Dis 88, 916-920.
70. Tairo, F., Mukasa, S. B., Jones, R. A. C., Kullaya, A., Rubaihayo, P. R. & Valkonen, J. P. T. (2005). Unraveling the genetic diversity of the three main viruses involved in Sweetpotato virus disease (SPVD), and its practical implications. Mol Plant Pathol 6, 199-211.
71. Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) sofware version 4.0. Mol Biol Evol 24, 1596-1599.
72. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
73. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876-4882.
74. Tomitaka, Y. & Ohshima, K. (2006). A phylogeographical study of the Turnip mosaic virus population in East Asia reveal an 'emergent' lineage in Japan. Mol Ecol 15, 4437-4457.
75. Torres-Barceló, C., Martín, S., Darós, J.-A. & Elena, S. F. (2008). From hypo- to hypersuppression: effect of amino acid substitutions on the RNA-silencing suppressor activity of the Tobacco etch virus HC-Pro. Genetics 180, 1039-1049.
76. Tugume, A. K., Mukasa, S. B. & Valkonen, J. P. T. (2008). Natural wild hosts of Sweetpotato feathery mottle virus show spatial differences in virus incidence and virus-like diseases in Uganda. Phytopathology 98, 640-652.
77. Valli, A., Martín-Hernández, A. M., López-Moya, J. J. & García, J. A. (2006). RNA silencing suppression by a second copy of the P1 serine proteinase of Cucumber vein yellowing ipomovirus, a member of the family Potyviridae that lacks the cysteine proteinase HCPro. J Virol 80, 10055-10063.
78. Valli, A., Lpez-Moya, J. J. & Garcia, J. A. (2007). Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88, 1016-1028.
79. Valli, A., Dujovny, G. & Garcia, J. A. (2008). Protease, self interaction, and small interfering RNA binding of the silencing suppressor P1b from Cucumber vein yellowing ipomovirus. J Virol 82, 974-986.
80. Valverde, R. A., Clark, C. A. & Valkonen, J. P. T. (2007). Viruses and virus disease complexes of sweetpotato. In Plant Viruses, vol. 1, pp. 116-126. London: Global Science Books.
81. Verchot, J., Herndon, K. L. & Carrington, J. C. (1992). Mutational analysis of the tobacco etch potyviral 35-kDa proteinase: identification of essential residues and requirements for autoproteolysis. Virology 190, 298-306.
82. Verdcourt, B. (1963). Convolvulaceae. In Flora of Tropical East Africa, pp. 1-161. Edited by C. E. Hubbard & E. Milne-Redhead. London: Whitefriars Press.
83. Wang, R. Y., Powell, G., Hardie, J. & Pirone, T. P. (1998). Role of the helper component in vector-specific transmission of potyviruses. J Gen Virol 79, 1519-1524.
84. Wang, W., Vignani, R., Scali, M. & Cresti, M. (2006). A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27, 2782-2786.
85. Wong, W. S. W., Yang, Z., Goldman, N. & Nielsen, R. (2004). Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168, 1041-1051.
86. Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003). An index of substitution saturation and its application. Mol Phylogenet Evol 26, 1-7.
87. Yang, Z. (2007). PAML4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24, 1586-1591.
88. Yang, Z., Nielsen, R., Goldman, N. & Pedersen, A. K. (2000). Codonsubstitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431-449.
89. Yang, Z., Wong, W. S. W. & Nielsen, R. (2005). Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22, 1107-1118.
90. Zhang, D., Rossel, G., Kriegner, A. & Hijmans, R. (2004). AFLP assessment of diversity in sweetpotato from Latin America and the Pacific region: its implications of the dispersal of the crop. Genet Resour Crop Evol 51, 115-120.