Abstract
To analyze the variation in rice black-streaked dwarf virus (RBSDV) in an area with high incidence of maize rough dwarf disease (MRDD), the RBSDV S1 segment in a collection of 100 maize isolates (sample population A100) from Jining, Shandong Province, was sequenced. An additional 21 maize and rice isolates (subpopulation B21) that were sampled from nine other geographic locations in China in 2012 and 2013 were used as a control. A total of 914 nucleotide mutations, including 239 singleton variable and 675 parsimony-informative sites were detected among the segment 1 (S1) sequences from A100. A total of 614 nucleotide mutation sites including 164 singleton variable and 450 parsimony-informative sites were detected among the S1 sequences from B21, while 97.55 % of the parsimony-informative sites from B21 were also detected in A100. The nucleotide sequence diversities of A100 (π = 0.0479) and B21 (π = 0.0396) were significantly different (P = 0.0002) but showed similar trends. Phylogenetic analysis showed that the 121 RBSDV isolates could be classified into two groups based on their S1 sequences, independent of subpopulation, with a combination of host species and locations. A100 and B21 were under the same level of negative and purifying selection, with Ka/Ks ratios of 0.0337 and 0.0369, respectively. The combined RBSDV population, including 121 isolates, was expanding, with negative values for Tajima’s D, Fu and Li’s D, and Fu and Li’s F in both A100 and B21, except Tajima’s D in A100. Based on S1, the RBSDV population in China has long-term phytogeographic stability, and there do not appear to be any newly-emerging strains.
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References
Carver TJ, Mullan LJ (2005) JAE: Jemboss Alignment Editor. Appl Bioinformatics 4:151–154
Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151:933–946
Dodds JA, Morris TJ, Jordan RL (1984) Plant viral double-stranded RNA. Annu Rev Phytopathol 22:151–168
Fang S, Yu J, Feng J, Han C, Li D, Liu Y (2001) Identification of rice black-streaked dwarf Fijivirus in maize with rough dwarf disease in China. Arch Virol 146:167–170
Hoang AT, Zhang HM, Yang J, Chen JP, Hebrard E, Zhou GH, Vien VN, Cheng JA, Chen JP (2011) Identification, characterization, and distribution of Southern rice black-streaked dwarf virus in Vietnam. Plant Dis 95:1063–1069
Hudson RR, Boss DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151
Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014
Kong XM, Jiang F, Zeng SM, Song CL, Han CW, Wu QP (2013) Occurrence and dynamics of small brown planthopper and control of maize rough dwarf disease with sowing date in maize. Crops 5:84–89
Li WH (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36:96–99
Li YQ, Jia MG, Jiang ZD, Zhou T, Fan ZF (2012) Molecular variation and recombination in RNA segment 10 of Rice black-streaked dwarf virus isolated from China during 2007–2010. Arch Virol 157:1351–1356
Li YQ, Xia ZH, Peng J, Zhou T, Fan ZF (2013) Evidence of recombination and genetic diversity in Southern rice black-streaked dwarf virus. Arch Virol 158:2147–2151
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lu HH, Sun QX, Peng CJ, Chen XH, Xue L, Hu JR, Chen GQ, Shi ML, Huang XL, Hao DR, Mao YX, Cheng YJ (2014) The effect of cause of maize rough dwarf disease and yield of fresh ear during different sowing. Jiangsu Agric Sci 41:75–76
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463
Martin S, Sambade A, Rubio L, Vives MC, Moya P, Guerri J, Elena SF, Moreno P (2009) Contribution of recombination and selection to molecular evolution of Citrus tristeza virus. J Gen Virol 90:1527–1538
Meng Y, Meng F, Han T, Liu K (2008) Causes and prevention measures of summer maize rough dwarf disease in Yellow and Huai River valleys of China. China Acad J 7:29–31
Milne RG, Conti M, Lisa V (1973) Partial purification, structure and infectivity of complete Maize rough dwarf virus particles. Virology 53:130–141
Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858
Pamilo P, Bianchi N (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10:271–281
Posada D, Crandall KA, Holmes EC (2002) Recombination in evolutionary genomics. Adv Virus Res 36:75–97
Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 537:337–350
Shackelton LA, Parrish CR, Holmes EC (1993) Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. J Mol Evol 62:551–563
Shi LY, Hao ZF, Weng JF, Xie CX, Liu CL, Zhang DG, Li MS, Bai L, Li XH, Zhang SH (2011) Identification of a major quantitative trait locus for resistance to Maize rough dwarf virus in a Chinese maize inbred line X178 using a linkage map based on 514 gene-derived single nucleotide polymorphisms. Mol Breed 30:615–625
Shi LY, Weng JF, Liu CL, Song XY, Miao HQ, Hao ZF, Xie CX, Li MS, Zhang DG, Bai L, Pan GT, Li XH, Zhang SH (2013) Identification of promoter motifs regulating ZmeIF4E expression level involved in maize rough dwarf disease resistance in maize (Zea Mays L.). Mol Genet Genomics 288:89–99
Su JD, Huang JB, Liu HS, Zhang JH (2008) Causes and prevention measures of maize rough dwarf disease in Yellow and Huai River valleys of China. China Acad J 23:169–170
Su JD, Huang JB, Liu HS, Ma JY, Hu YH (2009) Causes and prevention measures of maize rough dwarf disease in Yellow and Huai River valleys of China. Shandong Agric Sci 9:59–61
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tao YF, Liu QC, Wang HH, Zhang YJ, Huang XY, Wang BB, Lai JS, Ye JR, Liu BS, Xu ML (2013) Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease. BMC Plant Biol 13:145–157
Tomitaka Y, Ohshima K (2006) A phylogeographical study of the Turnip mosaic virus population in East Asia reveals an ‘emergent’ lineage in Japan. Mol Ecol 15:4437–4457
Valli A, Lopez-Moya JJ, Garcia JA (2007) Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88:1016–1028
Wang ZH, Fang SG, Xu JL, Sun LY, Li DW, Yu JL (2003) Sequence analysis of the complete genome of Rice black-streaked dwarf virus isolated from maize with rough dwarf disease. Virus Genes 27:163–168
Weng JF, Li B, Liu CL, Yang XY, Wang HW, Hao ZF, Li MS, Zhang DG, Ci XK, Li XH, Zhang SH (2013) A non-synonymous SNP within the isopentenyl transferase 2 locus is associated with kernel weight in Chinese maize inbreds (Zea mays L.). BMC Plant Biol 13:98–108
Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80:2535–2543
Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354
Yin X, Xu FF, Zheng FQ, Li XD, Liu BS, Zhang CQ (2011) Molecular characterization of segments S7 to S10 of a Southern rice black-streaked dwarf virus isolate from maize in northern China. Virol Sin 26:47–53
Yin X, Zheng FQ, Tang W, Zhu QQ, Li XD, Zhang GM, Liu HT, Liu BS (2013) Genetic structure of Rice black-streaked dwarf virus populations in China. Arch Virol 158:2505–2515
Zhang HM, Chen JP, Adams MJ (2001) Molecular characterisation of segments 1 to 6 of Rice black-streaked dwarf virus from China provides the complete genome. Arch Virol 146:2331–2339
Zhang HM, Chen JP, Lei JL, Adams MJ (2001) Sequence analysis shows that a dwarfing disease on rice, wheat and maize in China is caused by Rice black-streaked dwarf virus. Eur J Plant Pathol 107:563–567
Zhang HY, Diao YG, Yang HB, Zhao Y, Zhang XX, Zhai BP (2011) Population dynamics and migration characteristics of the small brown planthopper in spring in Jining. Chin J Appl Entomol 48:1298–1308
Zhang Y (2010) Characteristic and prevention measures of maize rough dwarf disease in coastal areas of Jiangsu province, China in 2009. China Acad J 23:171
Zhou Y, Weng JF, Chen YP, Liu CL, Han XH, Hao ZF, Li MS, Yong HJ, Zhang DG, Zhang SH, Li XH (2015) Phylogenetic and recombination analysis of Rice black-streaked dwarf virus segment 9 in China. Arch Virol 160:1119–1123
Zhou Y, Weng JF, Chen YP, Wu JR, Meng QC, Han XH, Hao ZF, Li MS, Yong HJ, Zhang DG, Zhang SH, Li XH (2015) Molecular genetic analysis and evolution of segment 7 in Rice black-streaked dwarf virus in China. PLoS One 10:e0131410
Acknowledgments
Plant samples were provided by Xiaomin Kong, Jianhua Yuan, Zhaodong Meng, Qi Sun, Tao Guo, Zhaowen Sun, Jie Shi, Wenyue Tong, Xiaohua Han, and Shuanggui Tie, whom we would like to thank for their kind assistance. This study was funded by the National Hi-Tech Research Program and Development Program of China (2012AA101104), the International Cooperation Program of Ministry of Science and Technology (2014DFG31690), the Science and Technology Program of Beijing (D141100005014003) and the Agricultural Science and Technology Innovation Program at CAAS. Author Jianfeng Weng has received research grants from the Chinese Academy of Agricultural Sciences. This article does not contain any studies with human participants or animals performed by any of the authors.
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Zhou, Y., Meng, Q., Chen, Y. et al. Molecular variation and expansion of a rice black-streaked dwarf virus population based on analysis of segment 1 in Jining, China. Arch Virol 161, 3435–3443 (2016). https://doi.org/10.1007/s00705-016-3052-z
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DOI: https://doi.org/10.1007/s00705-016-3052-z