Characterization of a new world monopartite begomovirus causing leaf curl Disease of Tomato in Ecuador and Peru Reveals a New Direction in Geminivirus Evolution

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5397-5413

  Melgarejo, Tomas A ^a,b   Kon, Tatsuya ^a,e   Rojas, Maria R ^a   Gilbertson, Robert L ^a   Zerbini, F Murilo ^c   Paz Carrasco, Lenin ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD NACIONAL AGRARIA LA MOLINA   (Peru)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^d INIAP   (Ecuador)

^e IWATE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ARTICLE; BEGOMOVIRUS; BINDING AFFINITY; BINDING SITE; C4 GENE; CONTROLLED STUDY; DNA SEQUENCE; ECUADOR; GEMINIVIRUS; GENETIC VARIABILITY; GENOTYPE; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PERU; PHENOTYPE; PHYLOGENY; PLANT LEAF; PLANT VIRUS; PRIORITY JOURNAL; TOMATO; TOMATO LEAF CURL DISEASE; TOMATO LEAF DEFORMATION VIRUS; VIRAL PLANT DISEASE; VIRUS GENE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS STRAIN;

BEGOMOVIRUS; DNA, VIRAL; ECUADOR; EVOLUTION, MOLECULAR; GENOME, VIRAL; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PERU; PLANT DISEASES; SEQUENCE ANALYSIS, DNA; TOBACCO;

EID: 84877621081     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00234-13     Document Type: Article

References (79)

1. Briddon RW, Patil BL, Bagewadi B, Nawaz-ul Rehman MS, Fauquet CM. 2010. Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evol. Biol. 10:97. doi:10 .1186/1471-2148-10-97.
2. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D. 1999. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. CRC Crit. Rev. Plant Sci. 18:71-106.
3. Harrison BD, Robinson DJ. 1999. Natural genomic and antigenic variation in whitefly-transmitted geminiviruses (begomoviruses). Annu. Rev. Phytopathol. 37:369-398.
4. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL. 2005. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43:361-394.
5. Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini FM, Zhou X. 2008. Geminivirus strain demarcation and nomenclature. Arch. Virol. 153:783-821.
6. Morales FJ. 2010. Distribution and dissemination of begomoviruses in Latin America and the Caribbean: Bemisia, p 283-318. In Stansly PA, Naranjo SE (ed), Bionomics and management of a global pest. Springer, London, United Kingdom.
7. Rojas MR, Gilbertson RL. 2008. Emerging plant viruses: a diversity of mechanisms and opportunities, p 27-51. In Roossinck MJ (ed), Plant virus evolution. Springer-Verlag, Berlin, Germany.
8. Seal SE, vanden Bosch F, Jeger MJ. 2006. Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. CRC Crit. Rev. Plant Sci. 25:23-46.
9. Saunders K, Salim N, Mali VR, Malathi VG, Briddon R, Markham PG, Stanley J. 2002. Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. Virology 293:63-74.
10. Gilbertson RL, Rojas MR, Natwick ET. 2011. Development of integrated pest management (IPM) strategies for whitefly (Bemisia tabaci)-transmissible geminiviruses, p 323-356. In Thompson WMO (ed), The whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) interactionwith geminivirus-infected host plants. Springer, Dordrecht, Netherlands.
11. Ha C, Coombs S, Revill P, Harding R, Vu M, Dale J. 2008. Molecular characterization of begomoviruses and DNA satellites from Vietnam: additional evidence that the New World geminiviruses were present in the Old World prior to continental separation. J. Gen. Virol. 89:312-326.
12. Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA, Meredith S, Lakay F, Monjane A, Lett JM, Varsani A, Heydarnejad J. 2010. The spread of Tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathog. 6:e1001164. doi:10.1371/journal.ppat.1001164.
13. Fiallo-OlivéE, Martínez-Zubiaur Y, Moriones E, Navas-Castillo J. 2012. Anovel class ofDNAsatellites associated with New World begomoviruses. Virology 426:1-6.
14. Paprotka T, Metzler V, Jeske H. 2010. The first DNA 1-like satellites in association with New World begomoviruses in natural infections. Virology 404:148-157.
15. Gutierrez C. 1999. Geminivirus DNA replication. Cell. Mol. Life Sci. 56:313-329.
16. Harrison BD, Swanson MM, Fargette D. 2002. Begomovirus coat protein: serology, variation and functions. Physiol. Mol. Plant Pathol. 60:257-271.
17. Sudarshana MR, Wang HL, Lucas WJ, Gilbertson RL. 1998. Dynamics of bean dwarf mosaic geminivirus cell-to-cell and long-distance movement in Phaseolus vulgaris revealed, using the green fluorescent protein. Mol. Plant Microbe Interact. 11:277-291.
18. Pooma W, Petty ITD. 1996. Tomato golden mosaic virus open reading frame AL4 is genetically distinct from its C4 analogue in monopartite geminiviruses. J. Gen. Virol. 77:1947-1951.
19. Polston JE, Anderson PK. 1997. The emergence of whitefly-transmitted geminiviruses in tomato in the Western hemisphere. Plant Dis. 81:1358-1369.
20. Zhou YC, Noussourou M, Kon T, Rojas MR, Jiang H, Chen LF, Gamby K, Foster R, Gilbertson RL. 2008. Evidence of local evolution of tomatoinfecting begomovirus species in West Africa: characterization of tomato leaf curl Mali virus and tomato yellow leaf crumple virus from Mali. Arch. Virol. 153:693-706.
21. Fernandes JJ, Carvalho MG, Andrade EC, Brommonschenkel SH, Fontes EPB, Zerbini FM. 2006. Biological and molecular properties of Tomato rugose mosaic virus (ToRMV), a new tomato-infecting begomovirus from Brazil. Plant Pathol. 55:513-522.
22. Rochester DE, DePaulo JJ, Fauquet CM, Beachy RN. 1994. Complete nucleotide sequence of the geminivirus Tomato yellow leaf curl virus, Thailand isolate. J. Gen. Virol. 75:477-486.
23. Guo W, Yang X, Xie Y, Cui X, Zhou X. 2009. Tomato yellow leaf curl Thailand virus-[Y72] from Yunnan is a monopartite begomovirus associated with DNA. Virus Genes 38:328-333.
24. Galvão RM, Mariano AC, Luz DF, Alfenas PF, Andrade EC, Zerbini FM, Almeida MR, Fontes EPB. 2003. A naturally occurring recombinant DNA-A of a typical bipartite begomovirus does not require the cognate DNA-B to infect Nicotiana benthamiana systemically. J. Gen. Virol. 84: 715-726.
25. Hou YM, Paplomatas EJ, Gilbertson RL. 1998. Host adaptation and replication properties of two bipartite geminiviruses and their pseudorecombinants. Mol. Plant Microbe Interact. 11:208-217.
26. Márquez-Martín B, Aragón-Caballero L, Fiallo-OlivéE, Navas-Castillo J, Moriones E. 2011. Tomato leaf deformation virus, a novel begomovirus associated with a severe disease of tomato in Peru. Eur. J. Plant Pathol. 129:1-7.
27. Murayama A, Aragon L, Fernandez-Northcote NE. 2005. Nuevo begomovirus del grupo del Nuevo Mundo asociado al encrespamiento de la hoja del tomate en la costa del Peru. Fitopatologia 40:1. (In Spanish.)
28. Gilbertson RL, Hidayat SH, Martinez RT, Leong SA, Faria JC, Morales F, Maxwell DP. 1991. Differentiation of bean-infecting geminiviruses by nucleic acid hybridization probes and aspects of bean golden mosaic in Brazil. Plant Dis. 75:336-342.
29. Rojas MR, Gilbertson RL, Russell DR, Maxwell DP. 1993. Use of degenerate primers in the polymerase chain reaction to detect whiteflytransmitted geminiviruses. Plant Dis. 77:340-347.
30. Dellaporta SL, Wood J, Hicks JB. 1983. A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1:19-21.
31. Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15.
32. Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG. 2002. Universal primers for the PCR-mediated amplification of DNA . Mol. Biotechnol.20:315-318.
33. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T. 2004. A simple method for cloning the complete begomovirus genome using the bacteriophage φ29 DNA polymerase. J. Virol. Methods 116:209-211.
34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
35. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.
36. Posada D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
37. Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
38. Martin DP. 2009. Recombination detection and analysis using RDP3. Methods Mol. Biol. 537:185-205.
39. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC. 1999. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J. Virol. 73:152-160.
40. Tajima F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460.
41. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
42. Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
43. Korber B. 2002. HIV signature and sequence variation analysis, p 55-72. In Rodrigo AG, LearnGH(ed), Computational analysis of HIV molecular sequences. Kluwer Academic Publishers, Boston, MA.
44. Zaaijer HL, van Hemert FJ, Koppelman MH, Lukashov VV. 2007. Independent evolution of overlapping polymerase and surface protein genes of hepatitis B virus. J. Gen. Virol. 88:2137-2143.
45. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. (Oxf.) 41:95-98.
46. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. 2009. Jalview version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191.
47. Hajdukiewicz P, Svab Z, Maliga P. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25:989-994.
48. Kon T, Gilbertson RL. 2012. Two genetically related begomoviruses causing tomato leaf curl disease in Togo and Nigeria differ in virulence and host range but do not require a betasatellite for induction of disease symptoms. Arch. Virol. 157:107-120.
49. Wise AA, Liu Z, Binns AN. 2006. Three methods for the introduction of foreign DNA into Agrobacterium. Methods Mol. Biol. 343:43-53.
50. Kon T, Rojas MR, Abdourhamane IK, Gilbertson RL. 2009. Roles and interactions of begomoviruses and satellite DNAs associated with okra leaf curl disease in Mali, West Africa. J. Gen. Virol. 90:1001-1013.
51. Wang HL, Gilbertson Rl, Lucas WJ. 1996. Spatial and temporal distribution of Bean dwarf mosaic geminivirus in Phaseolus vulgaris and Nicotiana benthamiana. Phytopathology 86:1204-1214.
52. Rojas MR, Jiang H, Salati R, Xoconostle-Cázares B, Sudarshana MR, Lucas WJ, Gilbertson RL. 2001. Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology 291:110-125.
53. Chen LF, Brannigan K, Clark R, Gilbertson RL. 2010. Characterization of curtoviruses associated with curly top disease of tomato in California and monitoring for these viruses in beet leafhoppers. Plant Dis. 94:99-108.
54. Arendt J, Reznick D. 2008. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23:26-32.
55. Carrillo-Tripp J, Lozoya-Gloria E, Rivera-Bustamante RF. 2007. Symptom remission and specific resistance of pepper plants after infection by Pepper golden mosaic virus. Phytopathology 97:51-59.
56. Hagen C, Rojas MR, Kon T, Gilbertson RL. 2008. Recovery from Cucurbit leaf crumple virus (family Geminiviridae, genus Begomovirus) infection is an adaptive antiviral response associated with changes in viral small RNAs. Phytopathology 98:1029-1037.
57. Zamir D, Ekstein-Michelson I, Zakay Y, Navot N, Zeidan M, Sarfatti M, Eshed Y, Harel E, Pleban T, Van-Oss H, Kedar N, Rabinowitch HD, Czosnek H. 1994. Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1. Theor. Appl. Genet. 88:141-146.
58. Rybicki EP. 1994. A phylogenetic and evolutionary justification for three genera of Geminiviridae. Arch. Virol. 139:49-77.
59. Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM. 2012. Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol. 61:457-467.
60. Gilbertson RL, Faria J, Ahlquist P, Maxwell DP. 1993. Genetic diversity in geminiviruses causing bean golden mosaic disease: the nucleotide sequence of the infectious cloned DNA components of a Brazilian isolate of bean golden mosaic geminivirus. Phytopathology 83:709-715.
61. Hagen C, Rojas MR, Sudarshana MR, Xoconostle-Cazares B, Natwick ET, Turini TA, Gilbertson RL. 2008. Biology and molecular characterization of Cucurbit leaf crumple virus, an emergent cucurbit-infecting begomovirus in the Imperial Valley of California. Plant Dis. 92:781-793.
62. Qazi J, Ilyas M, Mansoor S, Briddon RW. 2007. Legume yellow mosaic viruses: genetically isolated begomoviruses. Mol. Plant Pathol. 8:343-348. 63. Gutiérrez S, Michalakis Y, Blanc S. 2012. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr. Opin. Virol. 2:546-555.
63. Gutiérrez S, Michalakis Y, Blanc S. 2012. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr. Opin. Virol.2:546-555.
64. Qin S, Ward BM, Lazarowitz SG. 1998. The bipartite geminivirus coat protein aids BR1 function in viral movement by affecting the accumulation of viral single-stranded DNA. J. Virol. 72:9247-9256.
65. Zhou YC, Garrido-Ramirez ER, Sudarshana MR, Yendluri S, Gilbertson RL. 2007. The N-terminus of the begomovirus nuclear shuttle protein (BV1) determines virulence or avirulence in Phaseolus vulgaris. Mol. Plant Microbe Interact. 20:1523-1534.
66. Jupin I, De Kouchkovsky F, Jouanneau F, Gronenborn B. 1994. Movement of Tomato yellow leaf curl geminivirus (TYLCV): involvement of the protein encoded by ORF C4. Virology 204:82-90.
67. Amin I, Patil BL, Briddon RW, Mansoor S, Fauquet CM. 2011. Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virol. J. 8:238.
68. Dogra SC, Eini O, Rezaian MA, Randles JW. 2009. A novel shaggy-like kinase interacts with the Tomato leaf curl virus pathogenicity determinant C4 protein. Plant Mol. Biol. 71:25-38.
69. Raja P, Wolf JN, Bisaro DM. 2010. RNA silencing directed against geminiviruses: Post-transcriptional and epigenetic components. BBA Gen. Regul. Mech. 1799:337-351.
70. Tomás DM, Cañizares MC, Abad J, Fernández-Muñoz R, Moriones E. 2011. Resistance to Tomato yellow leaf curl virus accumulation in the tomato wild relative Solanum habrochaites associated with the C4 viral protein. Mol. Plant Microbe Interact. 24:849-861.
71. Vanitharani R, Chellappan P, Pita JS, Fauquet CM. 2004. Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J. Virol. 78:9487-9498.
72. Rodríguez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF. 2009. RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J. Virol. 83:1332-1340.
73. Chen L-F, Rojas M, Kon T, Gamby K, Xoconostle-Cazares B, Gilbertson RL. 2009. A severe symptom phenotype in tomato in Mali is caused by a reassortant between a novel recombinant begomovirus (Tomato yellow leaf curl Mali virus) and a betasatellite. Mol. Plant Pathol. 10:415-430.
74. Hou YM, Gilbertson RL. 1996. Increased pathogenicity in a pseudorecombinant bipartite geminivirus correlates with intermolecular recombination. J. Virol. 70:5430-5436.
75. Lefeuvre P, Lett JM, Varsani A, Martin DP. 2009. Widely conserved recombination patterns among single-stranded DNA viruses. J. Virol. 83: 2697-2707.
76. García-Andrés S, Accotto GP, Navas-Castillo J, Moriones E. 2007. 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 359:302-312.
77. Sanz AI, Fraile A, Gallego JM, Malpica JM, García-Arenal F. 1999. Genetic variability of natural populations of Cotton leaf curl geminivirus, a single-stranded DNA virus. J. Mol. Evol. 49:672-681.
78. Duffy S, Holmes EC. 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.
79. Duffy S, Shackelton LA, Holmes EC. 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9:267-276.