The Plant Pathology Journal

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

DOI QR Code

Whole-Genome Characterization of Alfalfa Mosaic Virus Obtained from Metagenomic Analysis of Vinca minor and Wisteria sinensis in Iran: with Implications for the Genetic Structure of the Virus

  • Moradi, Zohreh (Department of Plant Pathology, Faculty of Crop Sciences, Sari Agricultural Sciences and Natural Resources University) ;
  • Mehrvar, Mohsen (Department of Plant Pathology, Faculty of Agriculture, Ferdowsi University of Mashhad)
  • 투고 : 2021.10.13
  • 심사 : 2021.11.02
  • 발행 : 2021.12.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Alfalfa mosaic virus (AMV), an economically important pathogen, is present worldwide with a very wide host range. This work reports for the first time the infection of Vinca minor and Wisteria sinensis with AMV using RNA sequencing and reverse transcription polymerase chain reaction confirmation. De novo assembly and annotating of contigs revealed that RNA1, RNA2, and RNA3 genomic fragments consist of 3,690, 2,636, and 2,057 nucleotides (nt) for IR-VM and 3,690, 2,594, and 2,057 nt for IR-WS. RNA1 and RNA3 segments of IR-VM and IR-WS closely resembled those of the Chinese isolate HZ, with 99.23-99.26% and 98.04-98.09% nt identity, respectively. Their RNA2 resembled that of Canadian isolate CaM and American isolate OH-2-2017, with 97.96-98.07% nt identity. The P2 gene revealed more nucleotide diversity compared with other genes. Genes in the AMV genome were under dominant negative selection during evolution, and the P1 and coat protein (CP) proteins were subject to the strongest and weakest purifying selection, respectively. In the population genetic analysis based on the CP gene sequences, all 107 AMV isolates fell into two main clades (A, B) and isolates of clade A were further divided into three groups with significant subpopulation differentiation. The results indicated moderate genetic variation within and no clear geographic or genetic structure between the studied populations, implying moderate gene flow can play an important role in differentiation and distribution of genetic diversity among populations. Several factors have shaped the genetic structure and diversity of AMV: selection, recombination/reassortment, gene flow, and random processes such as founder effects.

키워드

과제정보

This work was supported by Sari Agricultural Sciences and Natural Resources University (No. 01-1400-03).

참고문헌

  1. Adams, I. P., Glover, R. H., Monger, W. A., Mumford, R., Jackeviciene, E., Navalinskiene, M., Samuitiene, M. and Boonham, N. 2009. Next-generation sequencing and metagenomic analysis: a universal diagnostic tool in plant virology. Mol. Plant Pathol. 10:537-545. https://doi.org/10.1111/j.1364-3703.2009.00545.x
  2. Al-Shahwan, I. M. 2002. Alfalfa mosaic virus (AMV) on alfalfa (Medicago sativa L.) in Saudi Arabia. Assiut J. Agric. Sci. 33:21-30.
  3. Bergua, M., Luis-Arteaga, M. and Escriu, F. 2014. Genetic diversity, reassortment, and recombination in Alfalfa mosaic virus population in Spain. Phytopathology 104:1241-1250. https://doi.org/10.1094/PHYTO-11-13-0309-R
  4. Bol, J. F. 1999. Alfalfa mosaic virus and ilarviruses: involvement of coat protein in multiple steps of the replication cycle. J. Gen. Virol. 80:1089-1102. https://doi.org/10.1099/0022-1317-80-5-1089
  5. Bol, J. F. 2008. Alfalfa Mosaic Virus. In: Encyclopedia of virology, 3rd ed., eds. by B. W. J. Mahy and M. H. V. van Regenmortel, pp. 81-87. Academic Press, Oxford, UK.
  6. Bonnet, J., Fraile, A., Sacristan, S., Malpica, J. M. and GarciaArenal, F. 2005. Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332:359-368. https://doi.org/10.1016/j.virol.2004.11.017
  7. Bujarski, J., Figlerowicz, M., Gallitelli, D., Roossinck, M. J. and Scott, S. W. 2012. Family Bromoviridae. In: Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses, eds. by A. M. Q. King, M. J. Adams, E. B. Carstens and E. J. Lefkowitz, pp. 965-976. Academic Press, Oxford, UK.
  8. Che, X., Jiang, X., Liu, X., Luan, X., Liu, Q., Cheng, X. and Wu, X. 2020. First report of Alfalfa mosaic virus on soybean in Heilongjiang, China. Plant Dis. 104:3085.
  9. Cuevas, J. M., Delaunay, A., Rupar, M., Jacquot, E. and Elena, S. F. 2012. Molecular evolution and phylogeography of potato virus Y based on the CP gene. J. Gen. Virol. 93:2496-2501. https://doi.org/10.1099/vir.0.044347-0
  10. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
  11. Edwardson, J. R. and Christie, R. G. 1997. Alfamovirus Genus. Alfalfa mosaic virus species. In: Viruses infecting peppers and other solanaceous crops, eds. by J. R. Edwardson and R. G. Christie, pp. 63-94. University of Florida Press, Gainesville, FL, USA.
  12. Esfandiari, N., Kohi Habibi, M., Mosahebi, G. H. and Mozafari, J. 2005. Detection of Alfalfa mosaic virus (AMV) in pea field in Iran. Commun. Agric. Appl. Biol. Sci. 70:407-410.
  13. Farahanikia, B., Akbarzadeh, T., Jahangirzadeh, A., Yassa, N., Shams Ardekani, M. R., Mirnezami, T., Hadjiakhoondi, A. and Khanavi, M. 2011. Phytochemical investigation of Vinca minor cultivated in Iran. Iran. J. Pharm. Res. 10:777-785.
  14. Fletcher, J. D. 2001. New hosts of Alfalfa mosaic virus, Cucumber mosaic virus, Potato virus Y, Soybean dwarf virus, and Tomato spotted wilt virus in New Zealand. N. Z. J. Crop Hortic. Sci. 29:213-217. https://doi.org/10.1080/01140671.2001.9514180
  15. Fu, Y. X. and Li, W. H. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709. https://doi.org/10.1093/genetics/133.3.693
  16. Gao, F., Lin, W., Shen, J. and Liao, F. 2016. Genetic diversity and molecular evolution of arabis mosaic virus based on the CP gene sequence. Arch. Virol. 161:1047-1051. https://doi.org/10.1007/s00705-015-2729-z
  17. Garcia-Arenal, F., Fraile, A. and Malpica, J. M. 2001. Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol. 39:157-186. https://doi.org/10.1146/annurev.phyto.39.1.157
  18. Golnaraghi, A. R., Shahraeen, N., Pourrahim, R., Farzadfar, S. and Ghasemi, A. 2004. Occurrence and relative incidence of viruses infecting soybeans in Iran. Plant Dis. 88:1069-1074. https://doi.org/10.1094/pdis.2004.88.10.1069
  19. Hamzeh, N., Koohi Habibi, M., Mosahebi, G., Dizadji, A. and Ghazanfari, K. 2010. Occurrence of Tomato spotted wilt virus, Cucumber mosaic virus and Alfalfa mosaic virus in Narcissus an ornamental plant in Iran. In: 19th Iranian Plant Protection Congress. Tehran, Iran.
  20. He, B., Fajolu, O. L., Wen, R.-H. and Hajimorad, M. R. 2010. Seed transmissibility of Alfalfa mosaic virus in soybean. Plant Health Prog. 11:41. https://doi.org/10.1094/php-2010-1227-01-br
  21. Herranz, M. C., Pallas, V. and Aparicio, F. 2012. Multifunctional roles for the N-terminal basic motif of Alfalfa mosaic virus coat protein: nucleolar/cytoplasmic shuttling, modulation of RNA-binding activity, and virion formation. Mol. PlantMicrobe Interact. 25:1093-1103. https://doi.org/10.1094/MPMI-04-12-0079-R
  22. Hiruki, C. and Hampton, R. O. 1990. Diseases caused by viruses and viruses infectious to alfalfa. In: Compendium of Alfalfa diseases, 2nd ed., eds. by D. L. Stuteville and D. C. Erwin, pp. 51-58. American Phytopathological Society, St. Paul, MN, USA.
  23. Houwing, C. J. and Jaspars, E. M. 1993. Coat protein stimulates replication complexes of Alfalfa mosaic virus to produce virion RNAs in vitro. Biochimie 75:617-621. https://doi.org/10.1016/0300-9084(93)90068-4
  24. Hudson, R. R. 2000. A new statistic for detecting genetic differentiation. Genetics 155:2011-2014. https://doi.org/10.1093/genetics/155.4.2011
  25. Jasper, E. M. J. and Bos, L. 1980. Alfalfa mosaic virus. Association of Applied Biologists Description of Plant Viruses N8 229. URL http://www.dpvweb.net/dpv/showdpv.php?dpvno=229 [3 November 2021].
  26. Jiang, Y., Chen, X., Lin, H., Wang, F. and Chen, F. 2011. Floral scent in wisteria: chemical composition, emission pattern, and regulation. J. Am. Soc. Hortic. Sci. 136:307-314. https://doi.org/10.21273/jashs.136.5.307
  27. Jukes, T. H. and Cantor, C. R. 1969. Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, ed. by H. N. Munro, pp. 21-132. Academic Press, New York, USA.
  28. Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549. https://doi.org/10.1093/molbev/msy096
  29. Maina, S., Zheng, L., Kinoti, W. M., Aftab, M., Nancarrow, N., Trebicki, P., King, S., Constable, F. and Rodoni, B. 2019. Metagenomic analysis reveals a nearly complete genome sequence of Alfalfa mosaic virus from a field pea in Australia. Microbiol. Resour. Announc. 8:e00766-19.
  30. Mangeli, F., Massumi, H., Alipour, F., Maddahian, M., Heydarnejad, J., Hosseinipour, A., Amid-Motlagh, M. H., Azizizadeh, M. and Varsani, A. 2019. Molecular and partial biological characterization of the coat protein sequences of Iranian Alfalfa mosaic virus isolates. J. Plant Pathol. 101:735-742. https://doi.org/10.1007/s42161-019-00275-w
  31. Martin, D. P., Murrell, B., Golden, M., Khoosal, A. and Muhire, B. 2015. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 1:vev003.
  32. Massumi, H., Maddahian, M., Heydarnejad, J., Hosseini Pour, A. and Farahmand, A. 2012. Incidence of viruses infecting alfalfa in the southeast and central regions of Iran. J. Agric. Sci. Technol. 14:1141-1148.
  33. Moradi, Z. and Mehrvar, M. 2019. Genetic variability and molecular evolution of Bean common mosaic virus populations in Iran: comparison with the populations in the world. Eur. J. Plant Pathol. 154:673-690. https://doi.org/10.1007/s10658-019-01690-6
  34. Neeleman, L., Linthorst, H. and Bol, J. F. 2004. Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3' termini of the viral RNAs. J. Gen. Virol. 85:231-240. https://doi.org/10.1099/vir.0.19581-0
  35. Pond, S. L. K. and Frost, S. D. W. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533. https://doi.org/10.1093/bioinformatics/bti320
  36. Pourrahim, R. and Farzadfar, S. 2015. Biological and molecular characterization of Alfalfa mosaic virus infecting trumpet creeper (Campsis radicans) in Iran. J. Phytopathol. 164:276-280. https://doi.org/10.1111/jph.12416
  37. Prabha, K., Baranwal, V. K. and Jain, R. K. 2013. Applications of next generation high throughput sequencing technologies in characterization, discovery and molecular interaction of plant viruses. Indian J. Virol. 24:157-165. https://doi.org/10.1007/s13337-013-0133-4
  38. Rozas, J., Ferrer-Mata, A., Sanchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E. and Sanchez-Gracia, A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34:3299-3302. https://doi.org/10.1093/molbev/msx248
  39. Sanchez-Navarro, J. A. and Bol, J. F. 2001. Role of the Alfalfa mosaic virus movement protein and coat protein in virus transport. Mol. Plant-Microbe Interact. 14:1051-1062. https://doi.org/10.1094/mpmi.2001.14.9.1051
  40. Sawalha, H. and Mansour, A. 1996. Incidence of Alfalfa mosaic virus in alfalfa fields in Jordan. Derasat 23:81-83.
  41. Smit, C. H. and Jaspars, E. M. 1982. Evidence that RNA 4 of Alfalfa mosaic virus does not replicate autonomously. Virology 117: 271-274. https://doi.org/10.1016/0042-6822(82)90528-1
  42. Song, S., Liu, H., Zhang, J., Pan, C. and Li, Z. 2019. Identification and characterization of complete genome sequence of Alfalfa mosaic virus infecting Gynostemma pentaphyllum. Eur. J. Plant Pathol. 154:491-497. https://doi.org/10.1007/s10658-018-01647-1
  43. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595. https://doi.org/10.1093/genetics/123.3.585
  44. Tenllado, F. and Bol, J. F. 2000. Genetic dissection of the multiple functions of Alfalfa mosaic virus coat protein in viral RNA replication, encapsidation, and movement. Virology 268:29-40. https://doi.org/10.1006/viro.1999.0170
  45. Thompson, J. D., Higgins, D. G. and Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. https://doi.org/10.1093/nar/22.22.4673
  46. United States Department of Agriculture. 2020. Vinca minor L.: common periwinkle. URL https://plants.usda.gov/home/plantProfile?symbol=VIMI2 [3 November 2021].
  47. van der Vossen, E. A. G., Neeleman, L. and Bol, J. F. 1994. Early and late functions of Alfalfa mosaic virus coat protein can be mutated separately. Virology 202:891-903. https://doi.org/10.1006/viro.1994.1411
  48. van Dun, C. M., Bol, J. F. and Van Vloten-Doting, L. 1987. Expression of Alfalfa mosaic virus and tobacco rattle virus coat protein genes in transgenic tobacco plants. Virology 159:299-305. https://doi.org/10.1016/0042-6822(87)90467-3
  49. Vas, A. and Gulyas, B. 2005. Eburnamine derivatives and the brain. Med. Res. Rev. 25:737-757. https://doi.org/10.1002/med.20043
  50. Weimer, J. L. 1931. Alfalfa mosaic virus. Phytopathology 21:122-123.
  51. Wright, S. 1951. The genetical structure of populations. Ann. Eugen. 15:323-354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x
  52. Wu, Q., Ding, S.-W., Zhang, Y. and Zhu, S. 2015. Identification of viruses and viroids by next-generation sequencing and homology-dependent and homology-independent algorithms. Annu. Rev. Phytopahol. 53:425-444. https://doi.org/10.1146/annurev-phyto-080614-120030
  53. Xu, H. and Nie, J. 2006. Identification, characterization, and molecular detection of Alfalfa mosaic virus in Potato. Phytopathology 96:1237-1242. https://doi.org/10.1094/PHYTO-96-1237
  54. Zenaddini, A., Jafarpour, B. and Falahati Rastegar, M. 2004. Identification and study on properties and distribution of Alfalfa mosaic virus in Khorasan province. In: 19th Iranian Plant Protection Congress. Tabriz, Iran.