Intrahost mechanisms governing emergence of resistance-breaking variants of Potato virus Y

Virology

Volumn 437, Issue 1, 2013, Pages 39-47

  Acosta Leal, Rodolfo ^a   Xiong, Zhongguo ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Cell to cell movement; Clonal interference; EIF4E; Hidden virulence; Potyvirus; Quasispecies; Random drift; Recessive resistance; Replicative fidelity; Selection

Indexed keywords

ADAPTATION; AMINO ACID SUBSTITUTION; ARTICLE; CISTRON; CONTROLLED STUDY; GENE MUTATION; GENOTYPE; HOST RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; POTYVIRUS; PRIORITY JOURNAL; TOBACCO; VIRUS GENE; VIRUS STRAIN; VIRUS VIRULENCE; VPG GENE;

GENETIC VARIATION; GENOTYPE; IMMUNITY, INNATE; MUTATION; PLANT DISEASES; POTYVIRUS; SERIAL PASSAGE; TOBACCO;

NICOTIANA TABACUM; POTATO VIRUS Y; POTYVIRUS;

EID: 84873077606     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.12.001     Document Type: Article

References (50)

1. Acosta-Leal R., Xiong Z. A plant resistance mechanism associated with the generation of resistance-breaking isolates of potato virus Y. Phytopathology 1994, 84:S1106.
2. Acosta-Leal R., Xiong Z. Complementary functions of two recessive R-genes determine resistance durability of tobacco 'Virgin A Mutant' (VAM) to Potato virus Y. Virology 2008, 379:275-283.
3. Athow K.L., Laviolette F.A., Wilcox J.R., Abney T.S. Registration of 'TN 86' Burley tobacco. Crop Sci. 1987, 27:365-366.
4. Ayme V., Petit-Pierre J., Souche S., Palloix A., Moury B. Molecular dissection of the Potato virus YVPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J. Gen. Virol. 2007, 88:1594-1601.
5. Blanco-Urgoiti B., Sánchez F., Pérez de San Román C., Dopazo J., Ponz F. Potato virus Y group C isolates are a homogeneous pathotype but two different genetic strains. J. Gen. Virol. 1998, 79:2037-2042.
6. Burch C.L., Chao L. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 2000, 406:625-628.
7. Burk L.G., Chaplin J.F., Gooding G.V., Powell N.T. Quantity production of anther-derived haploids from a multiple disease resistant tobacco hybrid. I. Frequency of plants with resistance or susceptibility to Tobacco mosaic virus (TMV), Potato virus Y (PVY) and root knot (RK)1. Euphytica 1979, 28:201-208.
8. Carrington J.C., Morris T.J. Complementary DNA cloning and analysis of Carnation mottle virus RNA. Virology 1984, 139:22-31.
9. Chaplin J.F., Burk L.G., Gooding G.V., Powell N.T. Registration of NC 744 tobacco germplasm. Crop Sci. 1980, 20:677.
10. De la Torre J.C., Holland J.J. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J. Virol. 1990, 64:6278-6281.
11. deVisser J.A.G.M., Zeyl C.W., Gerrish P.J., Blanchard J.L., Lenski R.E. Diminishing returns from mutation supply rate in asexual populations. Science 1999, 283:404-406.
12. Desbiez C., Gal-On A., Girard M., Wipf-Scheibel C., Lecoq H. Increase in Zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 2003, 93:1478-1484.
13. Drake J.W., Charlesworth B., Charlesworth D., Crow J.F. Rates of spontaneous mutations. Genetics 1998, 148:1667-1686.
14. Dullemans A.M., Cuperus C., Verbeek M., van der Vlugt R.A.A. Complete nucleotide sequence of a potato isolate of strain group C of Potato virus Y from 1938. Arch. Virol. 2011, 156:473-477.
15. Eigen M. On the nature of virus quasispecies. Trends Microbiol. 1996, 4:216-218.
16. Gibb K.S., Hellmann G.M., Pirone T.P. Nature of resistance of a tobacco cultivar to tobacco vein mottling virus. Mol. Plant-Microbe Interact. 1989, 2:332-339.
17. Gooding G.V. Relationship between strains of Potato virus Y and breeding for resistance, cross protection, and interference. Tob. Sci. 1985, 29:99-104.
18. Grzela R., Strokovska L., Andrieu J.P., Dublet B., Zagorski W., Chroboczek J. Potyvirus terminal protein VPg, effector of host eukaryotic initiation factor eIF4E. Biochimie 2006, 88:887-896.
19. Gupton C.L. Registration of Greeneville 107 Burley tobacco germplasm. Crop Sci. 1980, 20:116.
20. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
21. Janzac B., Fabre M.F., Palloix A., Moury B. Phenotype and spectrum of action of the Pvr4 resistance in pepper against potyviruses, and selection for virulent variants. Plant Pathol. 2009, 58:443-449.
22. Jenner C.E., Wang X.W., Ponz F., Walsh J.A. A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res. 2002, 86:1-6.
23. Jung J.-L., Bouzoubaa S., Gilmer D., Habne G. Visualization of transgene expression at the single protoplast level. Plant Cell Rep. 1992, 11:346-350.
24. Koelle G. Genetischeanalyseeiner Y-virus (Rippenbroun) resistantenmutante der tabaksorte Virgin A. Zuchter 1961, 31:71-72.
25. Lacroix C., Glais L., Verrier J.-L., Jacquot E. Effect of passage of a Potato virus Y isolate on a line of tobacco containing the recessive resistance gene va2 on the development of isolates capable of overcoming alleles 0 and 2. Eur J. Plant Pathol. 2011, 130:259-269.
26. Linch M. Evolution of the mutation rate. Trends Genet. 2010, 26:345-352.
27. Lommel S.A., McCain A.H., Morris T.J. Evaluation of indirect enzyme-linked immunosorbent assay for the detection of plant viruses. Phytopathology 1982, 72:1018-1022.
28. Lorenzen J.H., Meacham T., Berger P.H., Shiel P.J., Crosslin J.M., Hamm P.B., Kopp H. Whole genome characterization of Potato virus Y isolates collected in the western USA and their comparison to isolates from Europe and Canada. Arch. Virol. 2006, 151:1055-1074.
29. Masuta C., Nishimura M., Morishita H., Hataya T. A single amino acid change in viral genome-associated protein of Potato virus Y correlates with resistance breaking in 'Virgin A Mutant' tobacco. Phytopathology 1999, 89:118-123.
30. Miller C.R., Joyce P., Wichman H.A. Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 2011, 187:185-202.
31. Miralles R., Gerrish P.J., Moya A., Elena S.F. Clonal interference and the evolution of RNA viruses. Science 1999, 285:1745-1747.
32. Miralles R., Moya A., Elena S.F. Diminishing returns of population size in the rate of RNA virus adaptation. J. Virol. 2000, 74:3566-3571.
33. Mise K., Ahlquist P. Host-specificity restriction by bromovirus cell-to-cell movement protein occurs after initial cell-to-cell spread of infection in nonhost plants. Virology 1995, 206:276-286.
34. Miyashita S., Kishino H. Estimation of the size of genetic bottlenecks in cell-to-cell movement of soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements. J. Virol. 2010, 84:1828-1837.
35. Moreno I.M., Malpica J.M., Rodríguez-Cerezo E., García-Arenal F. A mutation in Tomato aspermycucumovirus that abolishes cell-to-cell movement is maintained to high levels in the viral RNA population by complementation. J. Virol. 1997, 71:9157-9162.
36. Moury B. A new lineage sheds light on the evolutionary history of Potato virus Y. Mol. Plant Pathol. 2010, 11:161-168.
37. Moury B., Morel C., Johansen E., Guilbaud L., Souche S., Ayme V., Caranta C., Palloix A., Jacquemond M. Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersiconhirsutum. Mol. Plant-Microbe Interact. 2004, 17:322-329.
38. Nicolas O., Dunnington S.W., Gotow L.F., Pirone T.P., Hellmann G.M. Variations in the VPg protein allow a potyvirus to overcome va gene resistance in tobacco. Virology 1997, 237:452-459.
39. Ojosnegros S., Beerenwinkel N., Antal T., Nowak M.A., Escamis C., Domingo E. Competition-colonization dynamics in an RNA virus. Proc. Natl. Acad. Sci. USA 2010, 107:2108-2112.
40. Poon A., Chao L. The rate of compensatory mutation in the DNA bacteriophage φX174. Genetics 2005, 170:989-999.
41. Rantalainen K.I., Eskelin K., Tompa P., Mäkinen K. Structural flexibility allows the functional diversity of potyvirus genome-linked protein VPg. J. Virol. 2011, 85:2449-2457.
42. Rantalainen K.I., Uversky V.N., Permi P., Kalkkinen N., Dunker A.K., Makinen K. Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 2008, 377:280-288.
43. Roudet-Tavert G., Michon T., Walter J., Delaunay T., Redondo E., Le Gall O. Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J. Gen. Virol. 2007, 88:1029-1033.
44. Sacristan S., Fraile A., Malpica J.M., Garcia-Arenal F. An analysis of host adaptation and its relationship with virulence in Cucumber mosaic virus. Phytopathology 2005, 95:827-833.
45. Sanjuán R., Nebot M.R., Chirico N., Mansky L.M., Belshaw R. Viral mutation rates. J. Virol. 2010, 84:9733-9748.
46. Sanz-Ramos M., Rodríguez-Calvo T., Sevilla N. Mutagenesis-mediated decrease of pathogenicity as a feature of the mutant spectrum of a viral population. PLoS ONE 2012, 7:e39941.
47. Teng M.N., Oldstone B.A., De La Torre J.C. Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by disease-negative virus variants. Virology 1996, 223:113-119.
48. Truniger V., Aranda M.A. Recessive resistance to plant viruses. Adv. Virus Res. 2009, 75:119-159.
49. Wilke C.O. Probability of fixation of an advantageous mutant in a viral quasispecies. Genetics 2003, 163:467-474.
50. Xiong Z., Lommel S.A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro from full-length cDNA clones. Virology 1991, 182:388-392.