The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Phylogenetic Characterization of Tomato chlorosis virus Population in Korea: Evidence of Reassortment between Isolates from Different Origins

  • Lee, Ye-Ji (Department of Genetic Engineering, Sungkyunkwan University) ;
  • Kil, Eui-Joon (Department of Genetic Engineering, Sungkyunkwan University) ;
  • Kwak, Hae-Ryun (Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration) ;
  • Kim, Mikyeong (Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration) ;
  • Seo, Jang-Kyun (Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration) ;
  • Lee, Sukchan (Department of Genetic Engineering, Sungkyunkwan University) ;
  • Choi, Hong-Soo (Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration)
  • Received : 2017.10.24
  • Accepted : 2018.02.16
  • Published : 2018.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Tomato chlorosis virus (ToCV) is a whitefly-transmitted and phloem-limited crinivirus. In 2013, severe interveinal chlorosis and bronzing on tomato leaves, known symptoms of ToCV infection, were observed in greenhouses in Korea. To identify ToCV infection in symptomatic tomato plants, RT-PCR with ToCV-specific primers was performed on leaf samples collected from 11 tomato cultivating areas where ToCV-like symptoms were observed in 2013 and 2014. About half of samples (45.18%) were confirmed as ToCV-infected, and the complete genome of 10 different isolates were characterized. This is the first report of ToCV occurring in Korea. The phylogenetic relationship and genetic variation among ToCV isolates from Korea and other countries were also analysed. When RNA1 and RNA2 are analysed separately, ToCV isolates were clustered into three groups in phylogenetic trees, and ToCV Korean isolates were confirmed to belong to two groups, which were geographically separated. These results suggested that Korean ToCV isolates originated from two independent origins. However, the RNA1 and RNA2 sequences of the Yeonggwang isolate were confirmed to belong to different groups, which indicated that ToCV RNA1 and RNA2 originated from two different origins and were reassorted in Yeonggwang, which is the intermediate point of two geographically separated groups.

Keywords

References

  1. Abou-Jawdah, Y., El Mohtar, C., Atamian, H. and Sobh, H. 2006. First report of Tomato chlorosis virus in Lebanon. Plant Dis. 90:378.
  2. Accotto, G., Vaira, A., Vecchiati, M., Finetti Sialer, M., Gallitelli, D. and Davino, M. 2001. First report of Tomato chlorosis virus in Italy. Plant Dis. 85:1208.
  3. Albuquerque, L. C., Varsani, A., Fernandes, F. R., Pinheiro, B., Martin, D. P., Ferreira, P. D. T. O., Lemos, T. O. and Inoue-Nagata, A. K. 2012. Further characterization of tomato-infecting begomoviruses in Brazil. Arch. Virol. 157:747-752. https://doi.org/10.1007/s00705-011-1213-7
  4. Alvarez-Ruiz, P., Jimenez, C., Leyva-Lopez, N. E. and Mendez-Lozano, J. 2007. First report of Tomato chlorosis virus infecting tomato crops in Sinaloa, Mexico. Plant Pathol. 56:1043. https://doi.org/10.1111/j.1365-3059.2007.01733_4.x
  5. Aranda, M. A., Fraile, A., Dopazo, J., Malpica, J. M. and Garcia-Arenal, F. 1997. Contribution of mutation and RNA recombination to the evolution of a plant pathogenic RNA. J. Mol. Evol. 44:81-88. https://doi.org/10.1007/PL00006124
  6. Arruabarrena, A., Rubio, L., Gonzalez-Arcos, M., Maeso, D., Fonseca, M. and Boiteux, L. 2015. First report of Tomato chlorosis virus infecting tomato crops in Uruguay. Plant Dis. 99:895.
  7. Barbosa, J., Teixeira, A., Moreira, A., Camargo, L., Filho, A. B., Kitajima, E. and Rezende, J. 2008. First report of Tomato chlorosis virus infecting tomato crops in Brazil. Plant Dis. 92:1709.
  8. Barbosa, J., Teixeira, L. and Rezende, J. 2010. First report on the susceptibility of sweet pepper crops to Tomato chlorosis virus in Brazil. Plant Dis. 94:374.
  9. Barton, H. D., Rohani, P., Stallknecht, D. E., Brown, J. and Drake, J. M. 2014. Subtype diversity and reassortment potential for co-circulating avian infuenza viruses at a diversity hot spot. J. Anim. Ecol. 83:566-575. https://doi.org/10.1111/1365-2656.12167
  10. Bese, G., Boka, K., Krizbai, L. and Takacs, A. 2011. First report of Tomato chlorosis virus in tomato from Hungary. Plant Dis. 95:363.
  11. Castro, R., Hernandez, E., Mora, F., Ramirez, P. and Hammond, R. 2009. First report of Tomato chlorosis virus in tomato in Costa Rica. Plant Dis. 93:970.
  12. Cevik, B. and EriB, G. 2008. First report of Tomato chlorosis virus in Turkey. Plant Pathol. 57:767-767.
  13. Dalmon, A., Bouyer, S., Cailly, M., Girard, M., Lecoq, H., Desbiez, C. and Jacquemond, M. 2005. First report of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato crops in France. Plant Dis. 89:1243.
  14. Domingo, E. and Holland, J. J. 1994. Mutation rates and rapid evolution of RNA viruses. In: The evolutionary biology of viruses, ed. S. S. Morse, pp. 161-184. Raven Press, NY, USA.
  15. Dovas, C., Katis, N. and Avgelis, A. 2002. Multiplex detection of criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Dis. 86:1345-1349. https://doi.org/10.1094/PDIS.2002.86.12.1345
  16. Fiallo-Olive, E., Hamed, A., Moriones, E. and Navas-Castillo, J. 2011. First report of Tomato chlorosis virus infecting tomato in Sudan. Plant Dis. 95:1592.
  17. Font, M., Juarez, M., Martinez, O. and Jorda, C. 2004. Current status and newly discovered natural hosts of Tomato infectious chlorosis virus and Tomato chlorosis virus in Spain. Plant Dis. 88:82.
  18. Fortes, I. M. and Navas-Castillo, J. 2012. Potato, an experimental and natural host of the crinivirus Tomato chlorosis virus. Eur. J. Plant Pathol. 134:81-86. https://doi.org/10.1007/s10658-012-0023-4
  19. Fuller, T. L., Gilbert, M., Martin, V., Cappelle, J., Hosseini, P., Njabo, K. Y., Aziz, S. A., Xiao, X., Daszak, P. and Smith, T. B. 2013. Predicting hotspots for infuenza virus reassortment. Emerg. Infect. Dis. 19:581-588. https://doi.org/10.3201/eid1904.120903
  20. Hanssen, I. M., Lapidot, M. and Thomma, B. P. 2010. Emerging viral diseases of tomato crops. Mol. Plant-Microbe Interact. 23:539-548. https://doi.org/10.1094/MPMI-23-5-0539
  21. Hirota, T., Natsuaki, T., Murai, T., Nishigawa, H., Niibori, K., Goto, K., Hartono, S., Suastika, G. and Okuda, S. 2010. Yellowing disease of tomato caused by Tomato chlorosis virus newly recognized in Japan. J. Gen. Plant Pathol. 76:168-171. https://doi.org/10.1007/s10327-010-0219-4
  22. Jacquemond, M., Verdin, E., Dalmon, A., Guilbaud, L. and Gognalons, P. 2009. Serological and molecular detection of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato. Plant Pathol. 58:210-220. https://doi.org/10.1111/j.1365-3059.2008.01959.x
  23. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnism, S. and Madden, T. L. 2008. NCBI BLAST: a better web interface. Nucleic Acids Res. 36:W5-W9. https://doi.org/10.1093/nar/gkn201
  24. Karasev, A. V. 2000. Genetic diversity and evolution of closteroviruses. Annu. Rev. Phytopathol. 38:293-324. https://doi.org/10.1146/annurev.phyto.38.1.293
  25. Kataya, A., Stavridou, E., Farhan, K. and Livieratos, I. 2008. Nucleotide sequence analysis and detection of a Greek isolate of Tomato chlorosis virus. Plant Pathol. 57:819-824. https://doi.org/10.1111/j.1365-3059.2008.01845.x
  26. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S. and Duran, C. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. https://doi.org/10.1093/bioinformatics/bts199
  27. 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. https://doi.org/10.1007/BF01731581
  28. Lett, J., Hoareau, M., Reynaud, B., Saison, A., Hostachy, B., Lobin, K. and Benimadhu, S. 2009. First report of Tomato chlorosis virus in tomato on Mauritius Island. Plant Dis. 93:111.
  29. Liu, H.-Y., Wisler, G. and Duffus, J. 2000. Particle lengths of whitefy-transmitted criniviruses. Plant Dis. 84:803-805. https://doi.org/10.1094/PDIS.2000.84.7.803
  30. Louro, D., Accotto, G. and Vaira, A. 2000. Occurrence and diagnosis of Tomato chlorosis virus in Portugal. Eur. J. Plant Pathol. 106:589-592. https://doi.org/10.1023/A:1008738130592
  31. Lozano, G., Moriones, E. and Navas-Castillo, J. 2004. First report of sweet pepper (Capsicum annuum) as a natural host plant for Tomato chlorosis virus. Plant Dis. 88:224.
  32. Lozano, G., Moriones, E. and Navas-Castillo, J. 2006. Complete nucleotide sequence of the RNA2 of the crinivirus Tomato chlorosis virus. Arch. Virol. 151:581-587. https://doi.org/10.1007/s00705-005-0690-y
  33. Marshall, N., Priyamvada, L., Ende, Z., Steel, J. and Lowen, A. C. 2013. Infuenza virus reassortment occurs with high frequency in the absence of segment mismatch. PLoS Pathog. 9:e1003421. https://doi.org/10.1371/journal.ppat.1003421
  34. Morris, J., Steel, E., Smith, P., Boonham, N., Spence, N. and Barker, I. 2006. Host range studies for Tomato chlorosis virus, and Cucumber vein yellowing virus transmitted by Bemisia tabaci (Gennadius). Eur. J. Plant Pathol. 114:265-273. https://doi.org/10.1007/s10658-005-5767-7
  35. Nagy, P. D. 2008. Recombination in plant RNA viruses. In: Plant virus evolution, pp. 133-156, Springer.
  36. Orílio, A. F., Fortes, I. M. and Navas-Castillo, J. 2014. Infectious cDNA clones of the crinivirus Tomato chlorosis virus are competent for systemic plant infection and whitefy-transmission. Virology 464:365-374.
  37. Rozen, S. and Skaletsky, H. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics Methods and Protocols. Methods in Molecular $Biology^{TM}$, vol 132, eds. by S. Misener and S. A. Krawetz, Humana Press, Totowa, NJ.
  38. Savory, F. R., Varma, V. and Ramakrishnan, U. 2014. Identifying geographic hot spots of reassortment in a multipartite plant virus. Evol. Appl. 7:569-579. https://doi.org/10.1111/eva.12156
  39. Segev, L., Wintermantel, W., Polston, J. and Lapidot, M. 2004. First report of Tomato chlorosis virus in Israel. Plant Dis. 88:1160.
  40. Simon, A. and Bujarski, J. 1994. RNA-RNA recombination and evolution in virus-infected plants. Annu. Rev. Phytopathol. 32:337-362. https://doi.org/10.1146/annurev.py.32.090194.002005
  41. Solorzano-Morales, A., Barboza, N., Hernandez, E., Mora-Umana, F., Ramirez, P. and Hammond, R. 2011. Newly discovered natural hosts of Tomato chlorosis virus in Costa Rica. Plant Dis. 95:497.
  42. Sundaraj, S., Srinivasan, R., Webster, C., Adkins, S., Perry, K. and Riley, D. 2011. First report of Tomato chlorosis virus infecting tomato in Georgia. Plant Dis. 95:881.
  43. Tamura, K. and Nei, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
  44. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  45. Thekke-Veetil, T., Polashock, J. J., Marn, M. V., Plesko, I. M., Schilder, A. C., Keller, K. E., Martin, R. R. and Tzanetakis, I. E. 2015. Population structure of blueberry mosaic associated virus: Evidence of reassortment in geographically distinct isolates. Virus Res. 201:79-84. https://doi.org/10.1016/j.virusres.2015.02.022
  46. Thompson, J. D., Gibson, T. and Higgins, D. G. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics 2:2.3.
  47. Trenado, H. P., Fortes, I. M., Louro, D. and Navas-Castillo, J. 2007. Physalis ixocarpa and P. peruviana, new natural hosts of Tomato chlorosis virus. Eur. J. Plant Pathol. 118:193-196. https://doi.org/10.1007/s10658-007-9129-5
  48. Tsai, W., Shih, S., Green, S., Hanson, P. and Liu, H. 2004. First report of the occurrence of Tomato chlorosis virus and Tomato infectious chlorosis virus in Taiwan. Plant Dis. 88:311.
  49. Vargas, J., Hammond, R., Hernandez, E., Barboza, N., Mora, F. and Ramírez, P. 2011. First report of Tomato chlorosis virus infecting sweet pepper in Costa Rica. Plant Dis. 95:1482.
  50. Vijaykrishna, D., Mukerji, R. and Smith, G. J. 2015. RNA virus reassortment: an evolutionary mechanism for host jumps and immune evasion. PLoS Pathog. 11:e1004902. https://doi.org/10.1371/journal.ppat.1004902
  51. Wille, M., Robertson, G. J., Whitney, H., Bishop, M. A., Runstadler, J. A. and Lang, A. S. 2011. Extensive geographic mosaicism in avian infuenza viruses from gulls in the northern hemisphere. PLoS One 6:e20664. https://doi.org/10.1371/journal.pone.0020664
  52. Wintermantel, W., Polston, J., Escudero, J. and Paoli, E. 2001. First report of Tomato chlorosis virus in Puerto Rico. Plant Dis. 85:228.
  53. Wintermantel, W., Wisler, G., Anchieta, A., Liu, H.-Y., Karasev, A. and Tzanetakis, I. 2005. The complete nucleotide sequence and genome organization of Tomato chlorosis virus. Arch. Virol. 150:2287-2298. https://doi.org/10.1007/s00705-005-0571-4
  54. Wintermantel, W. M. and Wisler, G. C. 2006. Vector specifcity, host range, and genetic diversity of Tomato chlorosis virus. Plant Dis. 90:814-819. https://doi.org/10.1094/PD-90-0814
  55. Wisler, G., Duffus, J., Liu, H.-Y. and Li, R. 1998a. Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Dis. 82:270-280. https://doi.org/10.1094/PDIS.1998.82.3.270
  56. Wisler, G., Li, R., Liu, H.-Y., Lowry, D. and Duffus, J. 1998b. Tomato chlorosis virus: a new whitefy-transmitted, phloemlimited, bipartite closterovirus of tomato. Phytopathology 88:402-409. https://doi.org/10.1094/PHYTO.1998.88.5.402
  57. Zhao, L.-M., Li, G., Gao, Y., Zhu, Y.-R., Liu, J. and Zhu, X.-P. 2015. Reverse transcription loop-mediated isothermal amplifcation assay for detecting Tomato chlorosis virus. J. Virol. Methods 213:93-97. https://doi.org/10.1016/j.jviromet.2014.11.013
  58. Zhao, L. M., Li, G., Gao, Y., Liu, Y. J., Sun, G. Z. and Zhu, X. P. 2014. Molecular detection and complete genome sequences of Tomato chlorosis virus isolates from infectious outbreaks in China. J. Phytopathol. 162:627-634. https://doi.org/10.1111/jph.12236
  59. Zhao, R., Wang, N., Wang, R., Chen, H., Shi, Y., Fan, Z. and Zhou, T. 2013a. Characterization and full genome sequence analysis of a Chinese isolate of Tomato chlorosis virus. Acta Virol. 58:92-94.
  60. Zhao, R., Wang, R., Wang, N., Fan, Z., Zhou, T., Shi, Y. and Chai, M. 2013b. First Report of Tomato chlorosis virus in China. Plant Dis. 97:1123.