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Genetic variability and molecular evolution of Bean common mosaic virus populations in Iran: comparison with the populations in the world

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Abstract

Bean common mosaic virus (BCMV) is an important plant pathogen causing considerable economic loss to legume production worldwide. In this study, the molecular characterizations of four BCMV isolates from Iran were determined, and their genetic variation and phylogenetic relationship compared with those of 49 other from GenBank. The genome contained a single open reading frame encoding a polyprotein of 3221, 3222, 3201 and 3202 amino acids (aa) in Ir-MSC1, Ir-GoB, Ir-MJB, and Ir-MSC2, respectively. Phylogenetic analysis of the polyprotein nucleotide sequences revealed that all 53 BCMV isolates clustered into six phylogroups distinguishable according to their genetic distances, namely S (soybean), P (peanut), C (common bean) and also three other distinct groups (R1, R2, and R3) of isolates all of which were recombinant. Iranian BCMV isolates did not form a compact group in the phylogenetic trees and shared 82.7–97.0% nt and 98.6–98.9% aa sequence identity among themselves and 80.1–98.7% nt and 83.4–99.8% aa sequence identity with the 49 other BCMV isolates. Of the 53 BCMV isolates studied, 34 (including Ir-MSC1 and Ir-GoB) were found to be recombinants at multiple regions of the genomes. The 19 non-recombinant isolates fell into three main phylogroups (S, P, and C) and tended to be classified according to their original host (with some exceptions). Statistically highly significant genetic differentiation (FST > 0.80) and infrequent gene flow were detected between the three phylogroups, suggesting ancestral differentiation. The normalized values for dN-dS indicated different purifying selection pressures acting on each of cistrons, with the P1 and NIa-Pro being subjected to the weakest and strongest functional constraints, respectively. Some codons (mainly in P1 and P3 regions) were under positive selection. This study presents a comprehensive analysis of evolutionary forces shaping the genetic structure of BCMV with implications for international exchanges of propagating materials.

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References

  • Adams, M. J., Antoniw, J. F., & Beaudoin, F. (2005). Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Molecular Plant Pathology, 6, 471–487.

    Article  CAS  PubMed  Google Scholar 

  • Arli-Sokmen, M., Deligoz, I., & Kutluk-Yilmaz, N. D. (2016). Characterization of Bean common mosaic virus and Bean common mosaic necrosis virus isolates in common bean growing areas in Turkey. European Journal of Plant Pathology, 146, 1–16.

    Article  CAS  Google Scholar 

  • Berger, P. H., Wyatt, S. D., Shiel, P. J., Silbernagel, M. J., Druffel, K., & Mink, M. I. (1997). Phylogenetic analysis of the Potyviridae with emphasis on legume-infecting potyviruses. Archives of Virology, 142, 1979–1999.

    Article  CAS  PubMed  Google Scholar 

  • Bitocchi, E., Nanni, L., Bellucci, E., Rossi, M., Giardini, A., Spagnoletti Zeuli, P., Logozzo, G., Stougaard, J., McClean, P., Attene, G. et al. (2012). Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proceedings of the National Academy of Sciences of the United States of America, Early Edition, 109(14), E788–796.

    Article  Google Scholar 

  • Bravo, E., Calverf, L. A., & Morales, F. J. (2008). The complete nucleotide sequence of the genomic RNA of Bean common mosaic virus strain NL4. Genetica, 32, 37–46.

    Google Scholar 

  • Chare, E. R., & Holmes, E. C. (2006). A phylogenetic survey of recombination frequency in plant RNA viruses. Archives of Virology, 151, 933–946.

    Article  CAS  PubMed  Google Scholar 

  • Chiquito-Almanza, E., Acosta-Gallegos, J. A., García-Álvarez, N. C., Garrido-Ramírez, E. R., Montero-Tavera, V., Guevara-Olvera, L., & Anaya-López, J. L. (2017). Simultaneous detection of both RNA and DNA viruses infecting dry bean and occurrence of mixed infections by BGYMV, BCMV and BCMNV in the central-west region of Mexico. Viruses, 9, e63.

    Article  CAS  PubMed  Google Scholar 

  • Chowda-Reddy, R. V., Sun, H., Chen, H., Poysa, V., Ling, H., Gijzen, M., & Wang, A. (2011). Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. Molecular Plant-Microbe Interactions, 24, 37–43.

    Article  CAS  PubMed  Google Scholar 

  • Chung, B. Y.-W., Miller, W. A., Atkins, J. F., & Firth, A. E. (2008). An overlapping essential gene in the Potyviridae. Proceedings of the National Academy of Sciences, USA, 105, 5897–5902.

    Article  CAS  Google Scholar 

  • Clark, M. F., & Adams, A. N. (1977). Characteristics of the micro plate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.

    Article  CAS  PubMed  Google Scholar 

  • Cronin, S., Verchot, J., Haldeman-Cahill, R., Schaad, M. C., & Carrington, J. C. (1995). Long-distance movement factor: A transport function of the potyvirus helper component proteinase. Plant Cell, 7, 549–559.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daròs, J. A., & Carrington, J. C. (1997). RNA binding activity of NIa proteinase of tobacco etch potyvirus. Virology, 237, 327–336.

    Article  PubMed  Google Scholar 

  • Daròs, J. A., Schaad, M. C., & Carrington, J. C. (1999). Functional analysis of the interaction between VPg-proteinase (NIa) and RNA polymerase (NIb) of tobacco etch potyvirus, using conditional and suppressor mutants. Journal of Virology, 73, 8732–8740.

    PubMed  PubMed Central  Google Scholar 

  • Dolja, V. V., Haldeman, R., Robertson, N. L., Dougherty, W. G., & Carrington, J. C. (1994). Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. The EMBO Journal, 13, 1482–1491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drijfhout, E., & Morales, F. (2005). Bean common mosaic. In H. F. Schwartz, J. R. Steadman, R. Hall, & R. L. Forster (Eds.), Compendium of bean diseases (Secondth ed., pp. 60–62). St. Paul: American Phytopathological Society.

    Google Scholar 

  • Drijfhout, E., Silbernagel, M. J., & Burke, D. W. (1978). Differentiation of strains of Bean common mosaic virus. Netherlands Journal of Plant Pathology, 84, 13–26.

    Article  Google Scholar 

  • Eggenberger, A., Hajimorad, M., & Hill, J. (2008). Gain of virulence on Rsv1-genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in both P3 and HC-pro. Molecular Plant-Microbe Interactions, 21, 931–936.

    Article  CAS  PubMed  Google Scholar 

  • Feng, X., Poplawsky, A. R., Nikolaeva, O. V., Myers, J. R., & Karasev, A. (2014a). Recombinants of Bean common mosaic virus (BCMV) and genetic determinants of BCMV involved in overcoming resistance in common bean. Phytopathology, 104, 786–793.

    Article  CAS  PubMed  Google Scholar 

  • Feng, X., Poplawsky, A. R., & Karasev, A. V. (2014b). A recombinant of Bean common mosaic virus induces temperature-insensitive necrosis in an I gene-bearing line of common bean. Phytopathology, 104, 1251–1257.

    Article  CAS  PubMed  Google Scholar 

  • Feng, X., Myers, J. R., & Karasev, A. (2015). Bean common mosaic virus isolate exhibits a novel pathogenicity profile in common bean, overcoming the bc-3 resistance allele coding for the mutated eIF4E translation initiation factor. Phytopathology, 105, 1487–1495.

    Article  CAS  PubMed  Google Scholar 

  • Flores-Estevez, N., Acosta-Gallegos, J. A., & Silva-Rosales, L. (2003). Bean common mosaic virus and Bean common mosaic necrosis virus in Mexico. Plant Disease, 87, 21–25.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Y. X., & Li, W. H. (1993). Statistical tests of neutrality of mutations. Genetics, 133, 693–709.

    CAS  PubMed  PubMed Central  Google Scholar 

  • García-Arenal, F., & McDonald, B. A. (2003). An analysis of the durability of resistance to plant viruses. Journal of Phytopathology, 93, 941–952.

    Article  Google Scholar 

  • García-Arenal, F., Fraile, A., & Malpica, J. M. (2001). Variability and genetic structure of plant virus populations. Annual Review of Phytopathology, 39, 157–186.

    Article  PubMed  Google Scholar 

  • Gepts, P., & Bliss, F. A. (1988). Dissemination paths of common bean (Phaseolus vulgaris, Fabaceae) deduced from phaseolin electrophoretic variability. II. Europe and Africa. Economic Botany, 42, 86–104.

    Article  Google Scholar 

  • Gepts, P., Osborn, T. C., Rashka, K., & Bliss, F. A. (1986). Phaseolin protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris)—Evidence for multiple centers of domestication. Economic Botany, 40, 451–468.

    Article  CAS  Google Scholar 

  • Gibbs, A. J., & Ohshima, K. (2010). Potyviruses and the digital revolution. Annual Review of Phytopathology, 48, 205–223.

    Article  CAS  PubMed  Google Scholar 

  • Gibbs, A. J., Ohshima, K., Phillips, M. J., & Gibbs, M. J. (2008a). The prehistory of Potyviruses: Their initial radiation was during the dawn of agriculture. PLoS One, 3, e2523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbs, A. J., Trueman, J. W., & Gibbs, M. J. (2008b). The Bean common mosaic virus lineage of potyviruses: where did it arise and when? Archives of Virology, 153, 2177–2187.

    Article  CAS  PubMed  Google Scholar 

  • Ha, C., Coombs, S., Revill, P. A., Harding, R. M., Vu, M., & Dale, J. L. (2008). Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Archives of Virology, 153, 25–36.

    Article  CAS  PubMed  Google Scholar 

  • Hampton, R. O., Silbernagel, M. J., & Burke, D. W. (1983). Bean common mosaic virus strains associated with bean mosaic epidemics in the northwestern United States. Plant Disease, 67, 658–661.

    Article  Google Scholar 

  • Hudson, R. R. (2000). A new statistic for detecting genetic differentiation. Genetics, 155, 2011–2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.

    Article  CAS  PubMed  Google Scholar 

  • Johary, T., Dizadji, A., & Naderpour, M. (2016). Biological and molecular characteristics of Bean common mosaic virus isolates circulating in common bean in Iran. Journal of Plant Pathology, 98, 301–310.

    Google Scholar 

  • Kim, B. M., Suehiro, N., Natsuaki, T., Inukai, T., & Masuta, C. (2010). The P3 protein of Turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI. Molecular Plant-Microbe Interactions, 23, 144–152.

    Article  CAS  PubMed  Google Scholar 

  • Klein, R. E., Wyatt, S. D., & Kaiser, W. J. (1988). Incidence of Bean common mosaic virus in USDA Phaseolus germ plasm collection. Plant Disease, 72, 301–302.

    Article  Google Scholar 

  • Koenig, R., & Gepts, P. (1989). Allozyme diversity in wild Phaseolus vulgaris: Further evidence for two major centers of genetic diversity. Theoretical and Applied Genetics, 78, 809–817.

    Article  CAS  PubMed  Google Scholar 

  • Larsen, R. C., Miklas, P. N., Druffel, K. L., & Wyatt, S. D. (2005). NL-3 K strain is a stable and naturally occurring interspecific recombinant derived from Bean common mosaic necrosis virus and Bean common mosaic virus. Phytopathology, 95, 1037–1042.

    Article  CAS  PubMed  Google Scholar 

  • Larsen, R. C., Druffel, K. L., & Wyatt, S. D. (2011). The complete nucleotide sequences of Bean common mosaic necrosis virus strains NL-5, NL-8 and TN-1. Archives of Virology, 156, 729–732.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y. Q., Liu, Z. P., Yang, Y. S., Zhao, B., Fan, Z. F., & Wan, P. (2014). First report of Bean common mosaic virus infecting azuki bean (Vigna angularis) in China. Plant Disease, 98, 1017.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Cao, Y., & Wan, P. (2016). Identification of a naturally occurring Bean common mosaic virus recombinant isolate infecting azuki bean. Journal of Plant Pathology, 98, 129–133.

    Google Scholar 

  • López, C., Aramburu, J., Galipienso, L., Soler, S., Nuez, F., & Rubio, L. (2011). Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus. Journal of General Virology, 92, 210–215.

    Article  CAS  PubMed  Google Scholar 

  • Maliogka, V. I., Salvador, B., Carbonell, A., Saenz, P., Leon, D. S., Oliveros, J. C., Delgadillo, M. O., Garcia, J. A., & Simon-mateo, C. (2012). Virus variants with differences in the P1 protein coexist in a Plum pox virus population and display particular host-dependent pathogenicity features. Molecular Plant Pathology, 13, 877–886.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, D. P., Murrell, B., Golden, M., Khoosal, A., & Muhire, B. (2015). RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1, vev003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez, F., Rodrigo, G., Aragones, V., Ruiz, M., Lodewijk, I., Fernandez, U., Elena, S. F., & Daros, J. A. (2016). Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection. BMC Genomics, 17, 87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mavric, I., & Sustar-Vozlic, J. (2004). Virus diseases and resistance to Bean common mosaic and Bean common mosaic necrosis potyvirus in common bean (Phaseolus vulgaris L.). Acta agriculturae slovenica, 83, 181–190.

    Google Scholar 

  • Mink, G. I., & Silbernagel, M. J. (1992). Serological and biological relationships among viruses in the Bean common mosaic virus subgroup. Archives of Virology. Supplementum, 5, 397–406.

    Article  CAS  PubMed  Google Scholar 

  • Moradi, Z., Mehrvar, M., Nazifi, E., & Zakiaghl, M. (2017). Iranian johnsongrass mosaic virus: the complete genome sequence, molecular and biological characterization, and comparison of coat protein gene sequences. Virus Genes, 53, 77–88.

    Article  CAS  PubMed  Google Scholar 

  • Morales, F. J., & Bos, L. (1988). Bean common mosaic virus. Descriptions of Plant Viruses, No. 337. http://www.dpvweb.net/dpv/showdpv.php?dpvno=337.

  • Muhire, B. M., Varsani, A., & Martin, D. P. (2014). SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One, 9, e108277. https://doi.org/10.1371/journal.pone.0108277.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy, J. F., Klein, P. G., Hunt, A. G., & Shaw, J. G. (1996). Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology, 220, 535–538.

    Article  CAS  PubMed  Google Scholar 

  • Naderpour, M., Mohammadi, M., Mossahebi, G. H., & Koohi Habibi, M. (2010). Identification of three strains of Bean common mosaic necrosis virus in common bean from Iran. Plant Disease, 94, 127.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa, T., Tomitaka, Y., Nakagawa, A., & Ohshima, K. (2008). Genetic structure of a population of Potato virus Y inducing potato tuber necrotic ringspot disease in Japan; comparison with north American and European populations. Virus Research, 131, 199–212.

    Article  CAS  PubMed  Google Scholar 

  • Ohshima, K., Yamaguchi, Y., Hirota, R., Hamamoto, T., Tomimura, K., Tan, Z., Sano, T., Azuhata, F., Walsh, J. A., & Fletcher, J. (2002). Molecular evolution of Turnip mosaic virus: Evidence of host adaptation, genetic recombination and geographical spread. Journal of General Virology, 83, 1511–1521.

    Article  CAS  PubMed  Google Scholar 

  • Olspert, A., Chung, B. Y., Atkins, J. F., Carr, J. P., Firth, A., & E. (2015). Transcriptional slippage in the positive-sense RNA virus family Potyviridae. EMBO Reports, e, 995–1004.

    Article  CAS  Google Scholar 

  • Parto, S., & Lartillot, N. (2018). Molecular adaptation in rubisco: Discriminating between convergent evolution and positive selection using mechanistic and classical codon models. PLoS One, 13, e0192697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Losada, M., Porter, M., & Crandall, K. A. (2008). Methods for analyzing viral evolution. In M. J. Roossinck (Ed.), Plant virus evolution (pp. 165–204). Berlin: Springer.

    Chapter  Google Scholar 

  • Pond, S. L. K., Frost, S. D. W., & Muse, S. V. (2005). HyPhy: Hypothesis testing using phylogenies. Bioinformatics, 21, 676–679.

    Article  CAS  PubMed  Google Scholar 

  • Revers, F., Le Gall, O., Candresse, T., & Maule, A. J. (1999). New advances in understanding the molecular biology of plant: Potyvirus interactions. Molecular Plant-Microbe Interactions, 12, 367–376.

    Article  CAS  Google Scholar 

  • Riechmann, J. L., Lain, S., & Garcia, J. A. (1992). Highlights and prospects of potyvirus molecular biology. Journal of General Virology, 73, 1–16.

    Article  CAS  PubMed  Google Scholar 

  • Rozas, J., Sanchez-DeI Barrio, J. C., Messeguer, X., & Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497.

    Article  CAS  PubMed  Google Scholar 

  • Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sanchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution, 34, 3299–3302.

    Article  CAS  PubMed  Google Scholar 

  • Saqib, M., Nouri, S., Cayford, B., Jones, R. A. C., & Jones, M. G. K. (2010). Genome sequences and phylogenetic placement of two isolates of Bean common mosaic virus from Macroptilium atropurpureum in north-West Australia. Australasian Plant Pathology, 39, 184–191.

    Article  CAS  Google Scholar 

  • Seo, J. K., Ohshima, K., Lee, H. G., Son, M., Choi, H. S., Lee, S. H., Sohn, S. H., & Kim, K. H. (2009). Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology, 393, 91–103.

    Article  CAS  PubMed  Google Scholar 

  • Shahraeen, N., Ghotbi, T., Dizaje, A., & Sahandi, A. (2005). A survey of viruses affecting French bean (Phaseolus vulgaris L.) in Iran includes a first report of Southern bean mosaic virus and Bean pod mottle virus. Plant Disease, 89, 1012.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, P., Sharma, P. N., Kapil, R., Sharma, S. K., & Sharma, O. P. (2011). Analysis of 3′-terminal region of Bean common mosaic virus strains infecting common bean in India. Indian Journal of Virology, 22, 37–43.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma, A., Sharma, V., Sharma, P., et al. (2016). Molecular characterization and genome organization of temperature insensitive necrosis inducing strain of BCMV infecting common bean in India. Australasian Plant Pathology, 45, 219–227.

    Article  CAS  Google Scholar 

  • Shukla, D. D., Jilka, J., Tosic, M., & Ford, R. E. (1989). A novel approach to the serology of potyviruses involving affinity-purified polyclonal antibodies directed towards virus specific N termini of coat proteins. Journal of General Virology, 70, 13–23.

    Article  CAS  Google Scholar 

  • Shukla, D. D., Lauricella, R., & Ward, C. W. (1992). Serology of potyviruses: current problems and some solutions. Archives of Virology. Supplementa, 5, 57–69.

    Article  CAS  Google Scholar 

  • Singh, S. P., & Schwartz, H. F. (2010). Breeding common bean for resistance to diseases. Review, 50, 2199–2223.

    Google Scholar 

  • Skotnicki, M. L., Mackenzie, A. M., & Gibbs, A. J. (1996). Genetic variation in populations of kennedya yellow mosaic tymovirus. Advances in Virology, 141, 99–110.

    CAS  Google Scholar 

  • Spence, N. J., & Walkey, D. G. A. (1995). Variation for pathogenicity among isolates of Bean common mosaic virus in Africa and reinterpretation of the genetic relationship between cultivars of Phaseolus vulgaris and pathotypes of BCMV. Plant Pathology, 44, 527–546.

    Article  Google Scholar 

  • Sztuba-Solińska, J., Urbanowicz, A., Figlerowicz, M., & Bujarski, J. J. (2011). RNA-RNA recombination in plant virus replication and evolution. Annual Review of Phytopathology, 49, 415–443.

    Article  CAS  PubMed  Google Scholar 

  • Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urcuqui-Inchima, S., Haenni, A., & Bernardi, F. (2001). Potyvirus proteins: a wealth of functions. Virus Research, 74, 157–175.

    Article  CAS  PubMed  Google Scholar 

  • Valli, A., Jose, J., pez-Moya, L., & Garcia, J. A. (2007). Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. Journal of General Virology, 88, 1016–1028.

    Article  CAS  PubMed  Google Scholar 

  • Van der Walt, E., Rybicki, E. P., Varsani, A., Polston, J. E., Billharz, R., Donaldson, L., Monjane, A. L., & Martin, D. P. (2009). Rapid host adaptation by extensive recombination. Journal of General Virology, 90, 734–746.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verchot, J., Koonin, E. V., & Carrington, J. C. (1991). The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. Virology, 185, 527–535.

    Article  CAS  PubMed  Google Scholar 

  • Verma, P., & Gupta, U. P. (2010). Immunological detection of Bean common mosaic virus in French bean (Phaseolusvulgaris L.) leaves. Indian Journal of Microbiology, 50, 263–265.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vetten, H., Green, S., & Lesemann, D. E. (1992). Characterization of Peanut stripe virus isolates from soybean in Taiwan. Journal of Phytopathology, 135, 107–124.

    Article  CAS  Google Scholar 

  • Wright, S. (1951). The genetical structure of populations. Annals of Eugenics, 15, 323–354.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, H., Chen, J., Chen, J., Adams, M. J., & Hou, M. (2002). Bean common mosaic virus isolates causing different symptoms in asparagus bean in China differ greatly in the 5′-parts of their genomes. Archives of Virology, 147, 1257–1262.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, G.-C., Wu, X.-Y., Zhang, Y.-M., Wu, P., Wu, X.-Z., Liu, L.-W., Wang, Q., Hang, Y.-Y., Yang, J.-Y., Shao, Z.-Q., Wang, B., & Chen, J. Q. (2014). A genomic survey of thirty soybean-infecting Bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Research, 191, 125–133.

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Plant Pathology, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Zohreh Moradi & Mohsen Mehrvar

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Moradi, Z., Mehrvar, M. 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 (2019). https://doi.org/10.1007/s10658-019-01690-6

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