Ferdowsi University of Mashhad

Document Type : Research Articles

Authors

1 Ferdowsi University of Mashhad, Mashhad, Iran

2 University of Mazandaran, Babolsar, Iran

Abstract

     Zucchini yellow mosaic virus (ZYMV) is one of the most economically important viruses infecting cucurbits worldwide. Population genetic analysis of ZYMV was conducted based on the virus cylindrical inclusion (CI) gene sequences of 10 isolates identified in this study and 94 other isolates from different countries in six continents: Asia, Europe, Oceania, Africa, North and South America. The overall mean value of nucleotide sequence diversity among all isolates was 0.074±0.006. Phylogenetic analysis showed that ZYMV isolates fell into three main phylogroups with significant FST values (>0.55) and almost tended to cluster according to their geographical position. Group I was predominant and contained isolates originated from different parts of the world. Iranian isolates clustered into group I, sharing 87.7-99.7% and 92.5–100% nucleotide and amino acid identity, with other isolates of this group. Group II was a new group that included only Singapore isolates. Group III including East Timor, Reunion Island and Australia-Kununurra isolates which were genetically differentiated from other populations. ZYMV populations from different geographic origins were composed of multiple lineages. With exception of the Oceanian population which was strongly differentiated from the American population, most other geographical populations showed low to moderate genetic differentiation. There was moderate to high level of gene flow despite large separating geographic distances. Analysis of the synonymous-to-nonsynonymous ratio showed strong purifying selection in the CI gene. The analyses indicated that in addition to selection, random processes such as genetic drift and founder effects are important determinants for the genetic structure of populations of ZYMV.

Keywords

Adams M.J., Antoniw J.F. and Beaudoin F. (2005a) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Molecular Plant Pathology 6:471–487.
Adams M.J., Antoniw J.F. and Fauquet C.M. (2005b) Molecular criteria for genus and species discrimination within the family Potyviridae. Archives of Virology 150:459–479.
Adams M.J., Zerbini F.M., French R., Rabenstein F., Stenger D.C. and Valkonen J.P.T. (2012) Family Potyviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. Virus taxonomy: Classification and nomenclature of viruses. Ninth report of the ICTV. London, UK: Academic Press, 1069–1089.
Al-Musa A.M. (1989) Over summering hosts for some cucurbit viruses in the Jordan Valley. Journal of Phytopathology 127:49–54.
Bananej K.A., Keshavarz T., Vahdat A., Hosseini Salekdeh G. and Glasa M.J. (2008) Biological and molecular variability of Zucchini yellow mosaic virus in Iran. Journal of Phytopathology 156:654-659.
Chen Y.K. and Hong Y.H. 2008. First report of Begonia chlorotic ringspot caused by Zucchini yellow mosaic virus in Taiwan. Plant Disease 92:1247.
Choi S.K., Yoon J.Y., Ryu K.H., Choi J.K. and Park W.M. (2002) First report of Zucchini yellow mosaic virus on hollyhock (Althaea rosea). Plant Pathology Journal 18:121–125.
Coutts B.A. and Jones R.A.C. (2005) Incidence and distribution of viruses infecting cucurbit crops in the Northern Territory and Western Australia. Australian Journal of Agricultural Research 56:847–858.
Coutts B.A., Kehoe M.A., Webster C.G., Wylie S.J. and Jones R.A. (2011) Zucchini yellow mosaic virus: biological properties, detection procedures and comparison of coat protein gene sequences. Archives of Virology 156:2119-31.
Chung BY-W., Miller W.A., Atkins J.F. and Firth A.E. (2008) An overlapping essential gene in the Potyviridae. Proceedings of the National Academy of Sciences of the USA 105:5897–5902.
Desbiez C., Wipf-Scheibel C., Granier F., Robaglia C., Delaunay T. and Lecoq H. (1996) Biological and molecular variability of Zucchini yellow mosaic virus in the island of Martinique. Plant Disease 80:203–207.
Desbiez C. and Lecoq H. (1997) Zucchini yellow mosaic virus. Plant Pathology 46: 809-829.
Desbiez C., Wipf-Scheibel C. and Lecoq H. (2002) Biological and serological variability, evolution and molecular epidemiology of Zucchini yellow mosaic virus (ZYMV, Potyvirus) with special reference to Caribbean islands. Virus Research 85:5–16.
Eagles D., Walker P.J., Zalucki M.P. and Durr P.A. (2013) Modelling spatio-temporal patterns of long-distance Culicoides dispersal into northern Australia. Preventive Veterinary Medicine 110: 312-322.
Gal-On A. (2007) Zucchini yellow mosaic virus: insect transmission and pathogenicity-the tails of two proteins. Molecular Plant Pathology 8:139–150.
Garcı´a-Arenal F., Fraile A. and Malpica J.M. (2003) Variation and evolution of plant virus populations. International Microbiology 6:225–232.
Gibbs A. and Ohshima K. (2010) Potyviruses and the digital revolution. Annual Review of Phytopathology 48: 205–223.
Glasa M., Svoboda J. and Novakova S. (2007) Analysis of the molecular and biological variability of Zucchini yellow mosaic virus isolates from Slovakia and Czech Republic. Virus Genes 35:415–421.
Ha C., Revill P., Harding R.M., Vu M. and Dale J.L. (2008a) Identification and sequence analysis of potyviruses infecting crops in Vietnam. Archives of Virology 153:45–60.
Ha C., Coombs S., Revill P.A., Harding R.M., Vu M. and Dale J.L. (2008b) Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Archives of Virology 153:25-36.
Hall T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.
Hudson R.R., Boos D.D. and Kaplan N.L. (1992a) A statistical test for detecting geographic subdivision. Molecular Biology and Evolution 9:138–151.
Hudson R.R., Slatkin M. and Maddison W.P. (1992b) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589.
Hudson R.R. (2000) A new statistic for detecting genetic differentiation. Genetics 155: 2011–2014.
Carrington J.C., Jensen P.E. and Schaad M.C. (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant Journal 14: 393–400.
Jukes T.H. and Cantor C.R. (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, NewYork, pp 21–132.
Klein P.G., Klein R.R., Rodriguez-Cerezo E., Hunt A.G. and Shaw J.G. (1994) Mutational analysis of the Tobacco vein mottling virus genome. Virology 204:759-769.
Kumar S., Stecher G., and Tamura K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870-1874.
Lecoq H., Pitrat M. and Clement M. (1981) Identification et caracterisation d’un potyvirus provoquant la maladie du rabougrissement jaune du melon. Agronomie 1:827–834.
Lecoq H., Bourdin D., Raccah B., Hiebert E. and Purcifull D.E. (1991) Characterization of a Zucchini yellow mosaic virus isolates with a deficient helper component. Phytopathology 81: 1087-1091.
Lecoq H., Desbiez C., Wipf-Scheibel C. and Girard M. (2003) Potential involvement of melon fruit in the long-distance dissemination of cucurbit potyviruses. Plant Disease 87:955–959.
Lee K.C., Mahtani P.H., Chng C.G. and Wong S.M. (1997) Sequence and phylogenetic analysis of the cytoplasmic inclusion protein gene of Zucchini yellow mosaic potyvirus: its role in classification of the Potyviridae. Virus Genes 14: 41–53.
Lisa V., Boccardo G., D’Agostino G., Dellavalle G. and d’Aquilio M. (1981) Characterization of a potyvirus that causes Zucchini yellow mosaic virus. Phytopathology 71: 667-672.
Lisa V. and Lecoq H. (1984) Zucchini yellow mosaic virus. CMI/AAB Description of Plant Viruses, No. 282.
Martin D.P., Murrell B., Golden M., Khoosal A. and Muhire B. (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Viral evolution 1:vev003.
Massumi H., Shaabanian M., Heydarnejad J., Hosseini Pour A. and Rahimian H. (2011) Host range and phylogenetic analysis of Iranian isolates of Zucchini yellow mosaic virus. Journal of Plant Pathology 93:187-193.
Maina S., Coutts B.A., Edwards O.R., Almeida L., Kehoe M.A., Ximenes A., and Jones R.A.C. (2017) Zucchini yellow mosaic virus populations from East Timorese and Northern Australian Cucurbit Crops: Molecular Properties, Genetic Connectivity, and Biosecurity Implications. Plant Disease 101:1236-1245.
Moury B., Morel C., Johansen E. and Jacquemond M. (2002) Evidence for diversifying selection in Potato virus Y and in the coat protein of other potyviruses. Journal of General Virology 83:2563- 2573.
Muhire B.M., Varsani A. and Martin D.P. (2014) SDT: A Virus Classification Tool Based on Pairwise Sequence Alignment and Identity Calculation. PLoS ONE 9: e108277.
Novakova S., Svoboda J. and Glasa M. (2014) Analysis of the complete sequences of two biologically distinct Zucchini yellow mosaic virus isolates further evidences the involvement of a single amino acid in the virus pathogenicity. Acta Virologica 58:364 – 367.
Riechmann J.L., Lain S. and Garcia J.A. (1992) Highlights and prospects of Potyvirus molecular biology. Journal of General Virology 73:1–16.
Rozas J., Sanchez-DeI Barrio J.C., Messeguer X. and Rozas R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497.
Rozas J., Ferrer-Mata A., S anchez-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 datasets. Molecular Biology and Evolution 34:3299-3302.
Schrijnwerkers C.C.F.M., Huijberts N. and Bos L. (1991) Zucchini yellow mosaic virus; two outbreaks in the Netherlands and seed transmissibility. Netherlands Journal of Plant Pathology 97:187–191.
Simmons H.E., Holmes E.C. and Stephenson A.G. (2008) Rapid evolutionary dynamics of Zucchini yellow mosaic virus. Journal of General Virology 89:1081–1085.
Simmons H.E., Holmes E.C., Gildow F.E., Bothe-Goralczyk M.A. and Stephenson A.G. (2011) Experimental Verification of Seed Transmission of Zucchini yellow mosaic virus. Plant Disease 95:751–754.
Simmons H.E., Dunham J.P., Zinn K.E., Munkvold G.P., Holmes E.C. and Stephenson A.G. (2013) Zucchini yellow mosaic virus (ZYMV, Potyvirus): Vertical transmission, seed infection and cryptic infections. Virus Research 176:259–264.
Tobias I. and Palkovics L. (2003) Characterization of Hungarian isolates of Zucchini yellow mosaic virus (ZYMV, Potyvirus) transmitted by seeds of Cucurbita pepo var. Styriaca. Pest Management Science 59:493–497.
Tsompana M., Abad J., Purugganan M. and Moyer J.W. (2005) The molecular population genetics of the Tomato spotted wilt virus (TSWV) genome. Molecular Ecology 14:53–66.
Urcuqui-Inchima S., Haenni A. and Bernardi F. (2001) Potyvirus proteins: a wealth of functions. Virus Research 74:157-175.
Wright S. (1951) The genetical structure of populations. Annals of eugenics 15:323–354.
Yakoubi S., Desbiez C., Fakhfakh H., Wipf-Scheibel C., Fabre F., Pitrat M., Marrakchi M. and Lecoq H. (2008) Molecular, biological and serological variability of Zucchini yellow mosaic virus in Tunisia. Plant Pathology 57:1146–1154.
Zhao M.F., Chen J., Zheng H.Y., Adams M.J. and Chen J.P. (2003) Molecular analysis of Zucchini yellow mosaic virus isolates from Hangzhou, China. Journal of Phytopathology 151:307-311.
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