Pepino mosaic virus: A successful pathogen that rapidly evolved from emerging to endemic in tomato crops

Molecular Plant Pathology

Volumn 11, Issue 2, 2010, Pages 179-189

  Hanssen, Inge M ^a   Thomma, Bart P H J ^b  

^a Scientia Terrae Research Institute   (Belgium)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CROP; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MOSAIC VIRUS; PHYSIOLOGY; PLANT DISEASE; STATISTICS; TOMATO; VIROLOGY; VIRUS GENOME; PLANT VIRUS; PREVENTION AND CONTROL; STATISTICS AND NUMERICAL DATA;

CROPS, AGRICULTURAL; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MOSAIC VIRUSES; PLANT DISEASES;

FLEXIVIRIDAE; LYCOPERSICON ESCULENTUM; MAGNOLIOPHYTA; PEPINO MOSAIC VIRUS; POTEXVIRUS; SOLANACEAE; SOLANUM; SOLANUM MURICATUM; URTICA;

EID: 75149152021     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00600.x     Document Type: Article

References (72)

1. Aguilar, J.M., Hernandez-Gallardo, M.D., Cenis, J.L., Lacasa, A. Aranda, M.A. (2002) Complete sequence of the Pepino mosaic virus RNA genome. Arch. Virol. 147, 2009 2015.
2. Alfaro-Fernández, A., Cebrián, M.C., Córdoba- Sellés, C., Herrera-Vásquez, J.A. Jordá, C. (2008) First report of the US1 strain of Pepino mosaic virus in tomato in the Canary Islands, Spain. Plant Dis. 92, 11.
3. Alfaro-Fernández, A., Córdoba-Selles, M.C., Herrera-Vásquez, J.A., Cebrián, M.C. Jordá, C. (2009) Transmission of Pepino mosaic virus by the fungal vector Olpidium virulentus. J. Phytopathol. doi: 10.1111/j.1439-0434.2009.01605.x.
4. Ascencio-Ibáñez, J.T., Sozzani, R., Lee, T.J., Chu, T.M., Wolfinger, R.D., Cella, R. Hanley-Bowdoin, L. (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting the pathogen response and cell cycle controls during geminivirus infection. Plant Physiol. 148, 436 454.
5. van Baarlen, P., van Esse, H.P., Siezen, R.J. Thomma, B.P.H.J. (2008) Challenges in plant cellular pathway reconstruction based on gene expression profiling. Trends Plant Sci. 13, 44 50.
6. Baulcombe, D. (2004) RNA silencing in plants. Nature, 431, 356 363.
7. Bhattacharjee, S., Zamora, A., Ahzar, M.T., Sacco, M.A., Lamber, L.H. Moffet, P. (2009) Virus resistance induced by NB-LRR proteins involves Argonaute4-dependent translational control. Plant J. 58, 940 951.
8. Córdoba, M.C., Martínez-Priego, L. Jordá, C. (2004) New natural hosts of Pepino mosaic virus in Spain. Plant Dis. 88, 906.
9. Córdoba-Sellés, M.C., García-Rández, A., Alfaro-Fernández, A. Jordá-Gutiérrez, C. (2007) Seed transmission of Pepino mosaic virus and efficacy of tomato seed disinfection treatments. Plant Dis. 91, 1250 1254.
10. Cotillon, A.C., Girard, M. Ducouret, S. (2002) Complete nucleotide sequence of the genomic RNA of a French isolate of Pepino mosaic virus (PepMV). Arch. Virol. 147, 2231 2238.
11. Davino, S., Accotto, G.P., Masenga, V., Torta, L. Davino, M. (2009) Basil (Ocimum basicilum), a new host of Pepino mosaic virus. Plant Pathol. 58, 407.
12. Desbiez, C. Lecoq, H. (1997) Zucchini yellow mosaic virus. Plant Pathol. 46, 809 829.
13. Ding, S.W. Voinnet, O. (2007) Antiviral immunity directed by small RNAs. Cell, 130, 413 426.
14. van Esse, H.P., Bolton, M.D., Stergiopoulos, I., de Wit, P.J.G.M. Thomma, B.P.H.J. (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol. Plant-Microbe Interact. 20, 1092 1101.
15. EPPO (2000) EPPO Alert list-viruses. Pepino mosaic potexvirus. http://www.eppo.org/QUARANTINE/Alert-List/viruses/PEPMV0.htm. [accessed on October 2009].
16. French, C.J., Bouthillier, M., Bernardy, M., Ferguson, G., Sabourin, M., Johnson, R.C., Masters, C., Godkin, S. Mumford, R. (2001) First report of Pepino mosaic virus in Canada and the United States. Plant Dis. 85, 1121.
17. Gal-On, A. Shiboleth, Y.M. (2006) Cross protection. In : Natural Resistance Mechanisms of Plants to Viruses (Loebenstein, G. Carr, J.P., eds), pp. 261 268. Dordrecht : Kluwer Academic Publishers.
18. Golemboski, D.B., Lomonossoff, G.P. Zaitlin, M. (1990) Plants transformed with tobacco mosaic virus nonstructural gene sequence are resistant to the virus. Proc. Natl. Acad. Sci. USA, 87, 6311 6315.
19. Gómez, P., Sempere, R.N., Elena, S.F. Aranda, M.A. (2009) Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J. Virol. doi: 10.1128/JVM.01486-09 (in press).
20. Gutiérrez-Aguirre, I., Mehle, N., Delic, D., Gruden, K., Mumford, R. Ravnikar, M. (2009) Real-time quantitative PCR based sensitive detection and genotype discrimination of Pepino mosaic virus. J. Virol. Methods, 162, 46 55.
21. Hanssen, I.M., Gutiérrez-Aguirre, I., Paeleman, A., Goen, K., Wittemans, L., Lievens, B., Vanachter, A.C.R.C., Ravnikar, M. Thomma, B.P.H.J. (2009c) Co-infection of greenhouse tomato with different Pepino mosaic virus isolates results either in cross-protection or enhanced symptom display. Plant Pathol. doi: 10.1111/j.1365-3059.2009.02190.x (in press).
22. Hanssen, I.M., Mumford, R., Blystad, D.-R., Cortez, I., Hasiów-jareszewska, B., Hristova, D., Pagán, I., Pepeira, A.-M., Peters, J., Pospieszny, H., Ravnikar, M., Stijger, I., Tomassoli, L., Varveri, C., van der Vlugt, R. Nielsen, S.L. (2009d) Seed transmission of Pepino mosaic virus in tomato. Eur. J. Plant Pathol. doi: 10.1007/s10658-009-9528-x.
23. Hanssen, I.M., Paeleman, A., Van Bergen, L., Vandewoestijne, E., Wittemans, L., Goen, K., Vanachter, A.C.R.C. Thomma, B.P.H.J. (2009a) Survey of symptom expression and damage caused by Pepino mosaic virus (PepMV) in commercial tomato production in Belgium. Acta Hort. 808, 185 192.
24. Hanssen, I.M., Paeleman, A., Vandewoestijne, E., Van Bergen, L., Bragard, C., Lievens, B., Vanachter, A.C.R.C. Thomma, B.P.H.J. (2009b) Pepino mosaic virus isolates and differential symptomatology in tomato. Plant Pathol. 58, 450 460.
25. Hanssen, I.M., Paeleman, A., Wittemans, L., Goen, K., Lievens, B., Bragard, C., Vanachter, A.C.R.C. Thomma, B.P.H.J. (2008) Genetic characterization of Pepino mosaic virus isolates from Belgian greenhouse tomatoes reveals genetic recombination. Eur. J. Plant Pathol. 121, 131 146.
26. Hasiów, B., Borodynko, N. Pospieszny, H. (2008) Complete genomic RNA sequence of the Polish Pepino Mosaic Virus isolate belonging to the US2 strain. Virus Genes, 36, 209 214.
27. Hasiów-Jaroszewska, B., Borodynko, N. Pospieszny, H. (2009b) Infectious RNA transcripts derived from cloned cDNA of a pepino mosaic virus isolate. Arch. Virol. 154, 853 856.
28. Hasiów-Jaroszewska, B., Pospieszny, H. Borodynko, N. (2009a) New necrotic isolates of Pepino mosaic virus representing the CH2 genotype. J. Phytopathol. 157, 494 496.
29. Jones, D.R. Lammers, W. (2005) Pest Risk Analysis for Pepino Mosaic Virus. York : Central Science Laboratory. http://www.defra.gov.uk/planth/pra.htm
30. Jones, R.A.C., Koenig, R. Lesemann, D.E. (1980) Pepino mosaic virus, a new potexvirus from pepino (Solanum muricatum). Ann. Appl. Biol. 94, 61 68.
31. Jordá, C., Lázaro-Perez, A. Martinez-Culebras, P.V. (2001) First report of Pepino mosaic virus on tomato in Spain. Plant Dis. 85, 1292.
32. Krinkels, M. (2001) PepMV causes sticky problem. Prophyta, May, 30 33.
33. Lacasa, A., Guerrero, M.M., Hita, I., Martinéz, M.A., Jordá, C., Bielza, P., Contreras, J., Alcázar, A. Cano, A. (2003) Implicationes de los abejorros (Bombus spp.) en la dipersión del virus del mosaico del pepino dulce (Pepino mosaic virus) en cultivos de tomato. Bol. Sanid. Veg., Plagas, 29, 393 402.
34. Lapidot, M., Gafny, R., Ding, B., Wolf, S., Lucas, W.J. Beachy, R.N. (1993) A dysfunctional movement protein of tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants. Plant J. 4, 959 970.
35. Ling, K. (2006) Molecular characterization of two Pepino mosaic virus variants from imported tomato seed reveals high levels of sequence identity between Chilean and US isolates. Virus Genes, 34, 1 8.
36. Ling, K. (2008) Pepino mosaic virus on tomato seed: virus location and mechanical transmission. Plant Dis. 9, 1701 1705.
37. Ling, K. Scott, J.W. (2007) Sources of resistance to Pepino mosaic virus in tomato accessions. Plant Dis. 91, 749 753.
38. Ling, K., Wechter, W.P. Jordan, R. (2007) Development of a one-step immunocapture real-time TaqMan RT-PCR assay for the broad spectrum detection of Pepino mosaic virus. J. Virol. Methods, 144, 65 72.
39. Ling, K., Wintermantel, W.M. Bledsoe, M. (2008) Genetic composition of Pepino mosaic virus population in North American greenhouse tomatoes. Plant Dis. 92, 1683 1688.
40. López, C., Soler, S. Nuez, F. (2005) Comparison of the complete sequences of three different isolates of Pepino mosaic virus: size variability of the TGBp3 protein between tomato and L. peruvianum isolates. Arch. Virol. 150, 619 627.
41. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H. Dinesh-Kumar, S.P. (2004) Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol. 55, 501 520.
42. Maroon-Lango, C.J., Guaragna, M.A., Jordan, R.L., Hammond, J., Bandla, M. Marquardt, S.K. (2005) Two unique US isolates of Pepino mosaic virus from a limited source of pooled tomato tissue are distinct from a third (EU like) US isolate. Arch. Virol. 150, 1187 1201.
43. Martin, J. Mousserion, C. (2002) Potato varieties which are sensitive to the tomato strains of Pepino mosaic virus (PepMV). Phytoma Défense Végétaux, 552, 26 28.
44. Maule, A., Leh, V. Lederer, C. (2002) The dialogue between viruses and host in compatible interactions. Curr. Opin. Plant Biol. 5, 1 6.
45. Mumford, R.A. Metcalfe, E.J. (2001) The partial sequencing of the genomic RNA of a UK isolate of Pepino mosaic virus and the comparison of the coat protein sequence with other isolates from Europe and Peru. Arch. Virol. 146, 2455 2460.
46. Pagán, I., Córdoba-Sellés, M.C., Martinez-Priego, L., Fraile, A., Malpica, J.M., Jordá, C. García-Arenal, F. (2006) Genetic structure of the population of Pepino mosaic virus infecting tomato crops in Spain. Phytopathology, 96, 274 279.
47. Pospieszny, H. Borodynko, N. (2006) New Polish isolates of Pepino mosaic virus highly distinct from European tomato, Peruvian and US2 strains. Plant Dis. 90, 1106.
48. Pospieszny, H., Borodynko, N. Palczewska, M. (2002) Occurrence of Pepino mosaic virus in Poland. Phytopathologia Polonica, 26, 91 94.
49. Pospieszny, H., Hasiów, B. Borodyndo, N. (2008) Characterization of two distinct Polish isolates of Pepino mosaic virus. Eur. J. Plant Pathol. 122, 443 445.
50. Prins, M., Laimer, M., Noris, E., Schubert, J., Wasseneger, M. Tepfer, M. (2008) Strategies for antiviral resistance in transgenic plants. Mol. Plant Pathol. 9, 73 83.
51. Quirino, B.F. Bent, A.F. (2003) Deciphering host resistance and pathogen virulence: the Arabidopsis/Pseudomonas interaction as a model. Mol. Plant Pathol. 4, 517 530.
52. Ratcliff, F.G., MacFarlane, S. Baulcombe, D.C. (1999) Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell, 11, 1207 1215.
53. Roggero, P., Masenga, V., Lenzi, R., Coghe, F., Ena, S. Winter, S. (2001) First report of Pepino mosaic virus in tomato in Italy. Plant Pathol. 50, 798.
54. Salomone, A. Roggero, P. (2002) Host range, seed transmission and detection by ELISA and lateral flow of an Italian isolate of Pepino mosaic virus. J. Plant Pathol. 84, 65 68.
55. Schwarz, D., Paschek, U., Bandte, M., Büttner, C. Obermeier, C. (2009) Detection, spread, and interactions of Pepino mosaic virus and Pythium aphanidermatum in the root environment of tomato in hydroponics. Acta Hort. 808, 163 170.
56. Senthil, G., Liu, H., Puram, V.G., Clark, A., Stromberg, A. Goodin, M.M. (2005) Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped virus. J. Gen. Virol. 86, 2615 2625.
57. Shipp, J.L., Buitenhuis, R., Stobbs, L., Wang, K., Kim, W.S. Ferguson, G. (2008) Vectoring of Pepino mosaic virus by bumble-bees in tomato greenhouses. Ann. Appl. Biol. 53, 149 155.
58. Soler, S., Cebolla-Cornejo, J., Prohens, J. Nuez, F. (2000) El Pepino Mosaic Virus (PepMV), una nueva amenaza para el cultivo del tomate. II. Vida Rural, 119, 48 52.
59. Soler, S., Prohens, J., Díez, M.J. Nuez, F. (2002) Natural occurrence of Pepino mosaic virus in Lycopersicon species in central and southern Peru. J. Phytopathol. 150, 49 53.
60. Soler-Aleixandre, S., López, C., Cebolla-Cornejo, J. Nuez, F. (2007) Sources of resistance to Pepino mosaic virus (PepMV) in tomato. HortScience, 42, 40 45.
61. Soler-Aleixandre, S., López, C., Díez, M.J., Pérez de Castro, A. Nuez, F. (2005) Association of Pepino mosaic virus with tomato collapse. J. Phytopathol. 153, 464 469.
62. Spence, N.J., Basham, J., Mumford, R.A., Hayman, G., Edmondson, R. Jones, D.R. (2006) Effect of Pepino mosaic virus on the yield and quality of glasshouse-grown tomatoes in the UK. Plant Pathol. 55, 595 606.
63. van der Vlugt, R.A.A., Stijger, C.C.M.M. Verhoeven, J.T.J. (2000) First report of Pepino Mosaic Virus on tomato. Plant Dis. 84, 103.
64. Verhoeven, J.T.J., van der Vlugt, R. Roenhorst, J.W. (2003) High similarity between tomato isolates of Pepino mosaic virus suggests a common origin. Eur. J. Plant Pathol. 109, 419 425.
65. Wang, H.L., Gonsalves, D., Provvidenti, R. Lecoq, H.L. (1991) Effectiveness of cross protection by a mild strain of zucchini yellow mosaic virus in cucumber, melon, and squash. Plant Dis. 75, 203 207.
66. Whitham, S.A., Quan, S., Chang, H.S., Cooper, B., Estes, B., Zhu, T., Wang, X. Hou, Y.M. (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J. 33, 271 283.
67. Whitham, S.A., Yang, C. Goodin, M.M. (2006) Global impact: elucidating plant responses to viral infection. Mol. Plant-Microbe Interact. 19, 1207 1215.
68. Wingard, S.A. (1928) Hosts and symptoms of ring spot, a virus disease of plants. J. Agric. Res. 37, 127 153.
69. Wise, R.P., Moscou, M.J., Bogdanove, A.J. Whitham, S.A. (2007) Transcript profiling in host-pathogen interactions. Annu. Rev. Phytopathol. 45, 329 369.
70. Wright, D. Mumford, R. (1999) Pepino mosaic Potexvirus (PepMV): first records in tomato in the United Kingdom. Plant Disease Notice No. 89. York: Central Science Laboratory.
71. Yaoliang, Z. Zhongjian, S. (2003) Preliminary characterization of Pepino mosaic virus Shanghai isolate (PepMV-Sh) and its detection with ELISA. Acta Agric. Shanghai, 19, 90 92.
72. Yeh, S.D. Gonsalves, D. (1984) Evaluation of induced mutants of Papaya ringspot virus for control by cross protection. Phytopathology, 74, 1086 1091.