Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin

Virology

Volumn 359, Issue 2, 2007, Pages 302-312

  García Andrés, Susana ^a   Accotto, Gian Paolo ^b   Navas Castillo, Jesús ^a   Moriones, Enrique ^a  

^a CSIC   (Spain)

^b INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

Begomovirus; Common bean; Founder effect; Genetic diversity; Mixed infections; Population structure; Recombination; Tomato; Tomato yellow leaf curl disease

Indexed keywords

ARTICLE; BEGOMOVIRUS; FOUNDER EFFECT; GENETIC RECOMBINATION; GEOGRAPHIC DISTRIBUTION; HOST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DISEASE; PLANT VIRUS; PRIORITY JOURNAL; STRAIN DIFFERENCE; TOMATO; TOMATO YELLOW LEAF CURL DISEASE; TOMATO YELLOW LEAF CURL MALAGA VIRUS; TOMATO YELLOW LEAF CURL SARDINIA VIRUS; TOMATO YELLOW LEAF CURL VIRUS; VIRUS MORPHOLOGY; VIRUS TYPING;

BEGOMOVIRUS; FABACEAE; FOUNDER EFFECT; GENOTYPE; LYCOPERSICON ESCULENTUM; MEDITERRANEAN REGION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT LEAVES; VARIATION (GENETICS);

BEGOMOVIRUS; LYCOPERSICON ESCULENTUM; TOMATO YELLOW LEAF CURL MALAGA VIRUS; TOMATO YELLOW LEAF CURL SARDINIA VIRUS; TOMATO YELLOW LEAF CURL VIRUS;

EID: 33847014211     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.09.030     Document Type: Article

References (79)

1. Accotto G.P., Navas-Castillo J., Noris E., Moriones E., and Louro D. Typing of tomato yellow leaf curl viruses in Europe. Eur. J. Plant Pathol. 106 (2000) 179-186
2. Accotto G.P., Bragaloni M., Luison D., Davino S., and Davino M. First report of Tomato yellow leaf curl virus (TYLCV) in Italy. Plant Pathol. 52 (2003) 799
3. Bebee T., and Rowe G. An Introduction to Molecular Ecology (2004), Oxford Univ. Press, Oxford
4. Bürger R. Evolution of genetic variability and the advantage of sex and recombination in changing environments. Genetics 153 (1999) 1055-1069
5. Crespi S., Noris E., Vaira A.M., and Accotto G.P. Molecular characterization of cloned DNA from a tomato yellow leaf curl virus isolate from Sicily. Phytopathol. Mediterr. 34 (1995) 93-99
6. Davino S., Napoli C., Davino M., and Accotto G.P. Spread of Tomato yellow leaf curl virus in Sicily: partial displacement of another geminivirus originally present. Eur. J. Plant Pathol. 114 (2006) 293-299
7. de Castro A.P., Díez M.J., and Nuez F. Evaluation of breeding tomato lines partially resistant to Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus derived from Lycopersicon chilense. Can. J. Plant Pathol. 27 (2005) 268-275
8. Elena S.F., and Sanjuan R. Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J. Virol. 79 (2005) 11555-11558
9. Fargette D., Pinel A., Abubakar Z., Traore O., Brugidou C., Fatogoma S., Hebrard E., Choisy M., Sere Y., Fauquet C., and Konate G. Inferring the evolutionary history of Rice yellow mottle virus from genomic, phylogenetic, and phylogeographic studies. J. Virol. 78 (2004) 3252-3261
10. Fauquet C.M., and Stanley J. Revising the way we conceive and name viruses below the species level: a review of geminivirus taxonomy calls for new standardized isolate descriptors. Arch. Virol. 150 (2005) 2151-2179
11. Fauquet C.M., Bisaro D.M., Briddon R.W., Brown J.K., Harrison B.D., Rybicki E.P., Stenger D.C., and Stanley J. Revision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species. Arch. Virol. 148 (2003) 405-421
12. Fauquet C.M., Sawyer S., Idris A.M., and Brown J.K. Sequence analysis and classification of apparent recombinant begomoviruses infecting tomato in the Nile and Mediterranean basins. Phytopathology 95 (2005) 549-555
13. Fitch W.M. Problem of discovering most parsimonious tree. Am. Nat. 111 (1977) 223-257
14. Fraile A., Alonso-Prados J.L., Aranda M.A., Bernal J.J., Malpica J.M., and García-Arenal F. Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J. Virol. 71 (1997) 934-940
15. García-Andrés S., Monci F., Navas-Castillo J., and Moriones E. Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350 (2006) 433-442
16. García-Arenal F., and McDonald B.A. An analysis of the durability of resistance to plant viruses. Phytopathology 93 (2003) 941-952
17. García-Arenal F., Fraile A., and Malpica J.M. Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol. 39 (2001) 157-186
18. Gibbs A.J., Keese P.L., Gibbs M.J., and García-Arenal F. Plant virus evolution: past, present and future. In: Domingo E., Webster R., and Holland J. (Eds). Origin and Evolution of Viruses (1999), Academic Press, New York 263-285
19. Gilbertson R.L., Rojas M.R., Russel D., and R. Maxwell D.P. Use of the asymmetric polymerase chain-reaction and DNA sequencing to determine genetic-variability of Bean golden mosaic geminivirus in the Dominican Republic. J. Gen. Virol. 7 (1991) 2843-2848
20. Gutierrez C. Geminivirus DNA replication. Cell. Mol. Life Sci. 56 (1999) 313-329
21. Hanley-Bowdoin L., Settlage S.B., Orozco B.M., Nagar S., and Robertson D. Geminiviruses: Models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 105-140
22. Heyraud-Nitschke F., Schumacher S., Laufs J., Schaefer S., Schell J., and Gronenborn B. Determination of the origin cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res. 23 (1995) 910-916
23. Hughes F.L., Rybicki E.P., and von Wechmar M.B. Genome typing of southern African subgroup I geminiviruses. J. Gen. Virol. 73 (1992) 1031-1040
24. Kheyr-Pour A., Bendahmane M., Matzeit V., Accotto G.P., Crespi S., and Gronenborn B. Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus. Nucleic Acids Res. 19 (1991) 6763-6769
25. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J. Mol. Evol. 16 (1980) 111-120
26. Kumar S., Tamura K., and Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5 (2004) 150-163
27. Lecoq H., Moury B., Desbiez C., Palloix A., and Pitrat M. Durable virus resistance in plants through conventional approaches: a challenge. Virus Res. 100 (2004) 31-39
28. Legg J.P., and Fauquet C.M. Cassava mosaic geminiviruses in Africa. Plant Mol. Biol. 56 (2004) 585-599
29. Li W.H. Unbiased estimation of the rates of synonymous and non-synonymous substitution. J. Mol. Evol. 36 (1993) 96-99
30. Lin C.S., Poushinsky G., and Mauer M. An examination of five sampling methods under random and clustered distribution using simulation. Can. J. Plant Sci. 59 (1979) 121-130
31. Martin D.P., Williamson C., and Posada D. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21 (2005) 260-262
32. Mastari J., Lapierre H., and Dessens J.T. Asymmetrical distribution of barley yellow dwarf virus PAV variants between host plant species. Phytopathology 88 (1998) 818-821
33. Moffat A.S. Plant pathology-Geminiviruses emerge as serious crop threat. Science 286 (1999) 1835
34. Monci F., Sánchez-Campos S., Navas-Castillo J., and Moriones E. A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303 (2002) 317-326
35. Morilla G., Antúnez C., Bejarano E.R., Janssen D., and Cuadrado I.M. A new Tomato yellow leaf curl virus strain in southern Spain. Plant Dis. 87 (2003) 1004
36. Morilla G., Janssen D., García-Andrés S., Moriones E., Cuadrado I.M., and Bejarano E.R. Pepper (Capsicum annuum), is a dead-end host for Tomato yellow leaf curl virus (TYLCV). Phytopathology 95 (2005) 1089-1097
37. Moriones E., and Navas-Castillo J. Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res. 71 (2000) 123-134
38. Moury B., Cardin L., Onesto J.P., Candresse T., and Poupet A. Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91 (2001) 84-91
39. Moya A., Holmes E.C., and Gonzalez-Candelas F. The population genetic and evolutionary epidemiology of RNA viruses. Nat. Rev. Microbiol. 2 (2004) 279-288
40. Navas-Castillo J., Sánchez-Campos S., Díaz J.A., Sáez-Alonso E., and Moriones E. Tomato yellow leaf curl virus-Is causes a novel disease of common bean and severe epidemics in tomato in Spain. Plant Dis. 83 (1999) 29-32
41. Navas-Castillo J., Sánchez-Campos S., Noris E., Louro D., Accotto G.P., and Moriones E. Natural recombination between Tomato yellow leaf curl virus-Is and Tomato leaf curl virus. J. Gen. Virol. 81 (2000) 2797-2801
42. Navot N., Pichersky E., Zeidan M., Zamir D., and Czosnek H. Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185 (1991) 151-161
43. Ndunguru J., Legg J.P., Aveling T.A.S., Thompson G., and Fauquet C.M. Molecular biodiversity of cassava begomoviruses in Tanzania: evolution of cassava geminiviruses in Africa and evidence for East Africa being a center of diversity of cassava geminiviruses. Virol. J. 2 (2005) 21
44. Nei M. Molecular Evolutionary Genetics (1987), Columbia Univ. Press, New York
45. Nei M., and Kumar S. Molecular Evolution and Phylogenetic (2000), Oxford Univ. Press, Oxford
46. Noris E., Hidalgo E., Accotto G.P., and Moriones E. High similarity among the tomato yellow leaf curl virus isolates from the West Mediterranean Basin: the nucleotide sequence of an infectious clone from Spain. Arch. Virol. 135 (1994) 165-170
47. Novella I.S., Elena S.F., Moya A., Domingo E., and Holland J.J. Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J. Virol. 69 (1995) 2869-2872
48. Ohshima K., Yamaguchi Y., Hirota R., Hamamoto T., Tomimura K., Tan Z.Y., Sano T., Azuhata F., Walsh J.A., Fletcher J., Chen J.S., Gera A., and Gibbs A.J. Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J. Gen. Virol. 83 (2002) 1511-1521
49. Ooi K., and Yahara T. Genetic variation of geminiviruses: comparison between sexual and asexual host plant populations. Mol. Ecol. 8 (1999) 89-97
50. Ooi K., Ohshita S., Ishii I., and Yahara T. Molecular phylogeny of geminivirus infecting wild plants in Japan. J. Plant Res. 110 (1997) 247-257
51. Orozco B.M., Miller A.B., Settlage S.B., and Hanley-Bowdoin L. Functional domains of a geminivirus replication protein. J. Biol. Chem. 272 (1997) 9840-9846
52. Padidam M., Sawyer S., and Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 265 (1999) 218-225
53. Pamilo P., and Bianchi N.O. Evolution of the ZFX and ZFY genes-rates and interdependence between the genes. Mol. Biol. Evol. 10 (1993) 271-281
54. Petty I.T.D., Carter S.C., Morra M.R., Jeffrey J.L., and Olivey H.E. Bipartite geminivirus host adaptation determined cooperatively by coding and noncoding sequences of the genome. Virology 277 (2000) 429-438
55. Pita J.S., Fondong V.N., Sangare A., Otim-Nape G.W., Ogwal S., and Fauquet C.M. Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J. Gen. Virol. 82 (2001) 655-665
56. Polston J.E., McGovern R.J., and Brown L.G. Introduction of tomato yellow leaf curl virus in Florida and implications for the spread of this and other geminiviruses of tomato. Plant Dis. 83 (1999) 984-988
57. Rojas M.R., Hagen C., Lucas W.J., and Gilbertson R.L. Exploting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43 (2005) 361-394
58. Roossinck M.J. Mechanisms of plant virus evolution. Annu. Rev. Phytopathol. 35 (1997) 191-209
59. Rubio L., Ayllón M.A., Kong P., Fernández A., Polek M., Guerri J., Moreno P., and Falk B.W. Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. J. Virol. 75 (2001) 8054-8062
60. Sacristán S., Fraile A., Malpica J.M., and García-Arenal F. An analysis of host adaptation and its relationship with virulence in Cucumber mosaic virus. Phytopathology 95 (2005) 827-833
61. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
62. Sánchez-Campos S., Navas-Castillo J., Camero R., Soria C., Díaz J.A., and Moriones E. Displacement of Tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89 (1999) 1038-1043
63. Sánchez-Campos S., Díaz J.A., Monci F., Bejarano E.R., Reina J., Navas-Castillo J., Aranda M.A., and Moriones E. High genetic stability of the begomovirus Tomato yellow leaf curl Sardinia virus in southern Spain over an 8-year period. Phytopathology 92 (2002) 842-849
64. Sanz A.I., Fraile A., Gallego J.M., Malpica J.M., and García-Arenal F. Genetic variability of natural populations of cotton leaf curl geminivirus, a single-stranded DNA virus. J. Mol. Evol. 49 (1999) 672-681
65. Schirmer A., Link D., Cognat V., Moury B., Beuve M., Meunier A., Bragard C., Gilmer D., and Lemaire O. Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. J. Gen. Virol. 86 (2005) 2897-2911
66. Schneider, S., Rossli, D., Excoffier, L., 2000. Arlequin: A software for population genetics data analysis. Version 2.0. Genetics and Biometry Laboratory, Department of Anthropology and Ecology, University of Geneva, Geneva. Switzerland. Available at http://lgb.unige.ch/arlequin/.
67. Seal S.E., vandenBosch F., and Jeger M.J. Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. Crit. Rev. Plant Sci. 25 (2006) 23-46
68. Sokal R.R., and Rolf F.J. Biometry. 2nd edn. (1981), Freeman, New York
69. Stanley J. 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 (1995) 707-712
70. Stanley J., Bisaro D.M., Briddon R.W., Brown J.K., Fauquet C.M., Harrison B.D., Rybicki E.P., and Stenger D.C. Geminiviridae. In: Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U., and Ball L.A. (Eds). Virus Taxonomy, VIIIth Report of the ICTV (2005), Elsevier/Academic Press, London 301-326
71. Stenger D.C., and McMahon C.L. Genotypic diversity of beet curly top virus populations in the western United States. Phytopathology 87 (1997) 737-744
72. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
73. Thompson J.R., Wetzel S., Klerks M.M., Vaskova D., Schoen C.D., Spak J., and Jelkmann W. Multiplex RT-PCR detection of four aphid-borne strawberry viruses in Fragaria spp. in combination with a plant mRNA specific internal control. J. Virol. Methods 111 (2003) 85-93
74. Tomimura K., Spak J., Katis N., Jenner C.E., Walsh J.A., Gibbs A.J., and Ohshima K. Comparisons of the genetic structure of populations of Turnip mosaic virus in West and East Eurasia. Virology 330 (2004) 408-423
75. Varma A., and Malathi V.G. Emerging geminivirus problems: a serious threat to crop production. Ann. Appl. Biol. 142 (2003) 145-164
76. Wartig L., Kheyr-Pour A., Noris E., Dekouchkovsky F., Jouanneau F., Gronenborn B., and Jupin I. Genetic analysis of the monopartite tomato yellow leaf curl geminivirus: roles of V1, V2, and C2 ORFs in viral pathogenesis. Virology 228 (1997) 132-140
77. Wright S. The interpretation of population structure by F-statistics with special regards to systems of mating. Evolution 19 (1965) 395-420
78. Yahara T., Ooi K., Oshita S., Ishii I., and Ikegami M. Molecular evolution of a host-range gene in geminiviruses infecting asexual populations of Eupatorium makinoi. Genes Genet. Syst. 73 (1998) 137-141
79. Yang Z.H., and Bielawski J.P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15 (2000) 496-503