Molecular characteristics of segment 5, a unique fragment encoding two partially overlapping ORFs in the genome of rice black-streaked dwarf virus

Autoři: Hongyue Zu aff001;  Hong Zhang aff001;  Minhao Yao aff001;  Jiayue Zhang aff001;  Hong Di aff001;  Lin Zhang aff001;  Ling Dong aff001;  Zhenhua Wang aff001;  Yu Zhou aff001
Působiště autorů: Key Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Northeast Agricultural University, Changjiang Road, Xiangfang District, Harbin, Heilongjiang Province, China aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224569


Rice black-streaked dwarf virus (RBSDV), a ds-RNA virus in Fijivirus genus with family Reoviridae, which is transmitted by the small brown planthopper, is responsible for incidence of maize rough dwarf disease (MRDD) and rice black-streaked dwarf disease (RBSDD). To understand the variation and evolution of S5, a unique fragment in the genome of RBSDV which encodes two partially overlapping ORFs (ORF5-1 and ORF5-2), we analyzed 127 sequences from maize and rice exhibiting symptoms of dwarfism. The nucleotide diversity of both ORF5-1 (π = 0.039) and ORF5-2 (π = 0.027) was higher than that of the overlapping region (π = 0.011) (P < 0.05). ORF5-2 was under the greatest selection pressure based on codon bias analysis, and its activation was possibly influenced by the overlapping region. The recombinant fragments of three recombinant events (14NM23, 14BM20, and 14NM17) cross the overlapping region. Based on neighbor-joining tree analysis, the overlapping region could represent the evolutionary basis of the full-length S5, which was classified into three main groups. RBSDV populations were expanding and haplotype diversity resulted mainly from the overlapping region. The genetic differentiation of combinations (T127-B35, T127-J34, A58-B35, A58-J34, and B35-J34) reached significant or extremely significant levels. Gene flow was most frequent between subpopulations A58 and B35, with the smallest |Fst| (0.02930). We investigated interactions between 13 RBSDV proteins by two-hybrid screening assays and identified interactions between P5-1/P6, P6/P9-1, and P3/P6. We also observed self-interactive effects of P3, P6, P7-1, and P10. In short, we have proven that RBSDV populations were expanding and the overlapping region plays an important role in the genetic variation and evolution of RBSDV S5. Our results enable ongoing research into the evolutionary history of RBSDV-S5 with two partly overlapping ORFs.

Klíčová slova:

DNA sequence analysis – Evolutionary genetics – Gene flow – Maize – Nucleotide sequencing – Protein interactions – Rice – Viral evolution


1. Yin X, Xu FF, Zheng FQ, Li XD, Liu BS, Zhang CQ. Molecular characterization of segments S7 to S10 of a southern rice black-streaked dwarf virus isolate from maize in northern China. Virol Sin. 2011; 26: 47–53. doi: 10.1007/s12250-011-3170-9 21331890

2. Xu QF, Ni HP, Zhang JF, Lan Y, Ren C, Zhou YJ. Whole-genome expression analysis of Rice black-streaked dwarf virus in different plant hosts and small brown planthopper. Gene. 2015; 572: 169–174. doi: 10.1016/j.gene.2015.07.008 26149652

3. Zhou Y, Zhang L, Zhang XM, Zu HY, Di H, Dong L, et al. Rice black-streaked dwarf virus Genome in China: Diversification, Phylogeny, and Selection. Plant Dis. 2017; 101: 1588–1596. doi: 10.1094/PDIS-12-16-1814-RE 30677338

4. Yang J, Zhang HM, Ying L, Li J, Lv MF, Xie L, et al. Rice black-streaked dwarf virus genome segment S5 is a bicistronic mRNA in infected plants. Arch Virol. 2014; 159: 307–314. doi: 10.1007/s00705-013-1832-2 24013236

5. Li J, Xue J, Zhang HM, Yang J, Lv MF, Xie L, et al. Interactions between the P6 and P5-1 proteins of southern rice black-streaked dwarf fijivirus in yeast and plant cells. Arch Virol. 2013; 158: 1649–1659. doi: 10.1007/s00705-013-1660-4 23474918

6. Liu XY, Yang J, Xie L, Li J, Song XJ, Chen JP, et al. P5-2 of rice black-streaked dwarf virus is a non-structural protein targeted to chloroplasts. Arch Virol. 2015; 160: 1211–1217. doi: 10.1007/s00705-015-2382-6 25749897

7. Steinhauer DA, Holland JJ. Rapid evolution of RNA viruses. Annu. Rev. Microbiol. 1987, 41: 409–33. doi: 10.1146/annurev.mi.41.100187.002205 3318675

8. Walia JJ, Willemsen A, Elci E, Caglayan K, Falk BW, Rubio L. Genetic Variation and Possible Mechanisms Driving the Evolution of Worldwide Fig mosaic virus Isolates. Phytopathology. 2014; 104(1). doi: 10.1094/PHYTO-05-13-0145-R 24571394

9. Acosta-Leal R, Duffy S, Xiong Z, Hammond RW, Elena SF. Advances in Plant Virus Evolution: Translating Evolutionary Insights into Better Disease Management. Phytopathology. 2011; 101(10). doi: 10.1094/PHYTO-01-11-0017 21554186

10. Mertens P. The dsRNA viruses. VIRUS RES. 2004; 101(1): 3–13. doi: 10.1016/j.virusres.2003.12.002 15010213

11. Ge BB, He Z, Zhang ZX, Wang HQ, Li SF. Genetic variation in potato virus M isolates infecting pepino (Solanum muricatum) in China. Arch Virol. 2014; 159: 3197–3210. doi: 10.1007/s00705-014-2180-6 25233939

12. Sun BJ, Sun LY, Tugume AK, Adams MJ, Yang J, Xie LH, et al. Selection pressure and founder effects constrain genetic variation in differentiated populations of soilborne bymovirus Wheat yellow mosaic virus (Potyviridae) in China. Phytopathology. 2013; 103: 949–59. doi: 10.1094/PHYTO-01-13-0013-R 23550972

13. Nouri S, Arevalo R, Falk BW, Groves RL. Genetic structure and molecular variability of Cucumber mosaic virus isolates in the United States. PLoS One. 2014; 9: 1–12. doi: 10.1371/journal.pone.0096582 24801880

14. Roossinck MJ. Mechanisms of plant virus evolution. ANNU REV PHYTOPATHOL. 1997; 35: 191–209. doi: 10.1146/annurev.phyto.35.1.191 15012521

15. Datta S. An overview of molecular epidemiology of hepatitis B virus (HBV) in India. Virol J. 2008; 5: 156. doi: 10.1186/1743-422X-5-156 19099581

16. Ding SW, Anderson BJ, Haase HR, Symons RH. New overlapping gene encoded by the cucumber mosaic virus genome. Virology. 1994; 198: 593–601. doi: 10.1006/viro.1994.1071 8291242

17. Salaipeth L, Chiba S, Eusebio-Cope A, Kanematsu S, Suzuki N. Biological properties and expression strategy of rosellinia necatrix megabirnavirus 1 analysed in an experimental host, Cryphonectria parasitica. J Gen Virol. 2014; 95: 740–750. doi: 10.1099/vir.0.058164-0 24259190

18. Du ZY, Chen FF, Liao QS, Zhang HR, Chen YF, Chen JS. 2b ORFs encoded by subgroup IB strains of cucumber mosaic virus induce differential virulence on Nicotiana species. J Gen Virol. 2007; 88: 2596–2604. doi: 10.1099/vir.0.82927-0 17698672

19. Seo JK, Ohshima K, Lee HG, Son M, Choi HS, Lee SH, et al. Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology. 2009; 393: 91–103. doi: 10.1016/j.virol.2009.07.007 19716150

20. Carver TJ, Mullan LJ. JAE: Jemboss Alignment Editor. Appl Bioinformatics. 2005; 4(2): 151–4. 16128618

21. Li YQ, Jia MG, Jiang ZD, Zhou T, Fan ZF. Molecular variation and recombination in RNA segment 10 of rice black-streaked dwarf virus isolated from China during 2007–2010. Arch Virol. 2012; 157(7): 1351–6. doi: 10.1007/s00705-012-1282-2 22447103

22. Ma HX, Pan JJ, Kang K, Xie ZQ, Ru WP, Chen HM, et al. [Genome sequences of coxsackievirus B5 isolated from viral encephalitis patients in Henan province, 2011]. Zhonghua Liu Xing Bing Xue Za Zhi. 2013; 34(12): 1213–5. 24518022

23. Weng JF, Li B, Liu CL, Yang XY, Wang HW, Hao ZF, et al. A non-synonymous SNP within theisopentenyl transferase2 locus is associated with kernel weight in Chinese maize inbreds (Zea mays L.). BMC Plant Biol. 2013; 13: 98–108. doi: 10.1186/1471-2229-13-98 23826856

24. Wright F. The effective number of codons used in a gene. Gene. 1990; 87(1): 23–9. doi: 10.1016/0378-1119(90)90491-9 2110097

25. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016; 33(7): 1870–4. doi: 10.1093/molbev/msw054 27004904

26. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015; 1(1):1–5. doi: 10.1093/ve/vev001 27774277

27. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25(11):1451–2. doi: 10.1093/bioinformatics/btp187 19346325

28. Wright S. The genetical structure of populations. Ann Eugen. 1951; 15(4): 323–54. 24540312

29. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003; 19(18):2496–7. doi: 10.1093/bioinformatics/btg359 14668244

30. Wei TY, Yang JG, Liao FR, Gao FL, Lu LM, Zhang XT, et al. Genetic diversity and population structure of rice stripe virus in China. J Gen Virol. 2009; 90: 1548. doi: 10.1099/vir.0.006858–0 19264655

31. Li RG, Song W, Wang BQ, Wang JH, Zhang DM, Zhang QG, et al. Identification of a locus conferring dominant resistance to maize rough dwarf disease in maize. Sci Rep. 2018; 8(1): 3248. doi: 10.1038/s41598-018-21677-3 29459698

32. Shi LY, Hao ZF, Weng JF, Xie CX, Liu CL, Zhang DG, et al. 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 BREEDING. 2012; 30: 615–625. doi: 10.1007/s11032-011-9652-0

33. Tao YF, Liu QC, Wang HH, Zhang YJ, Huang XY, Wang BB, et al. Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease. BMC Plant Biol. 2013; 13: 145. doi: 10.1186/1471-2229-13-145 24079304

34. Yin X, Zheng FQ, Tang W, Zhu QQ, Li XD, Zhang GM, et al. Genetic structure of rice black-streaked dwarf virus populations in China. Arch Virol. 2013; 158(12): 2505–15. doi: 10.1007/s00705-013-1766-8 23807744

35. Zhou Y, Weng JF, Chen YP, Liu CL, Han XH, Hao ZF, et al. Phylogenetic and recombination analysis of rice black-streaked dwarf virus segment 9 in China. Arch Virol. 2015; 160(4):1119–23. doi: 10.1007/s00705-014-2291-0 25633210

36. Jenkins GM, Holmes EC. The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res. 2003; 92(1): 1–7. doi: 10.1016/s0168-1702(02)00309-x 12606071

37. Gupta SK, Ghosh TC. Gene expressivity is the main factor in dictating the codon usage variation among the genes in Pseudomonas aeruginosa. Gene. 2001; 273(1):63–70. doi: 10.1016/s0378-1119(01)00576-5 11483361

38. Chiusano ML, Alvarez-Valin F, Di Giulio M, D'Onofrio G, Ammirato G, Colonna G, et al. Second codon positions of genes and the secondary structures of proteins. Relationships and implications for the origin of the genetic code. doi: 10.1016/s0378-1119(00)00521-7 PMID: 11164038

39. Xie T, Ding DF. The relationship between synonymous codon usage and protein structure. FEBS Lett. 1998; 434(1–2): 93–6. doi: 10.1016/s0014-5793(98)00955-7 9738458

40. Cardinale DJ, DeRosa K, Duffy S. Base composition and translational selection are insufficient to explain codon usage bias in plant viruses. Viruses. 2013; 5(1): 162–81. doi: 10.3390/v5010162 23322170

41. McInerney JO. Replicational and transcriptional selection on codon usage in Borrelia burgdorferi. Proc Natl Acad Sci U S A. 1998; 95(18): 10698–703. doi: 10.1073/pnas.95.18.10698 9724767

42. Chen WH, Lu G, Bork P, Hu S, Lercher MJ. Energy efficiency trade-offs drive nucleotide usage in transcribed regions. Nat Commun. 2016; 7: 11334. doi: 10.1038/ncomms11334 27098217

43. Lynn DJ, Singer GAC, Hickey DA. Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res. 2002; 30(19): 4272–7. doi: 10.1093/nar/gkf546 12364606

44. Kanamori Y, Nakashima N. A tertiary structure model of the internal ribosome entry site (IRES) for methionine-independent initiation of translation. RNA. 2001; 7(2): 266–74. doi: 10.1017/s1355838201001741 11233983

45. Chare ER, Holmes EC, 2006. A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol. 2006; 151(5): 933–46. doi: 10.1007/s00705-005-0675-x 16292597

46. Valli A, López-Moya JJ, García JA. Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol. 2007; 88: 1016–28. doi: 10.1099/vir.0.82402-0 17325376

47. Worobey M, Holmes EC. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999; 80: 2535–43. doi: 10.1099/0022-1317-80-10-2535 10573145

48. Azzam O, Yambao MLM, Muhsin M, McNally KL, Umadhay KML. Genetic diversity of rice tungro spherical virus in tungro-endemic provinces of the Philippines and Indonesia. Arch Virol. 2000; 145(6): 1183–97. doi: 10.1007/s007050070118 10948991

49. Li J, Xue J, Zhang HM, Yang J, Xie L, Chen JP. Characterization of homologous and heterologous interactions between viroplasm proteins P6 and P9-1 of the fijivirus southern rice black-streaked dwarf virus. Arch Virol. 2015; 160(2): 453–7. doi: 10.1007/s00705-014-2268-z 25377635

50. Zhang LD, Wang ZH, Wang XB, Li DW, Han CG, Zhai YF, et al. Two virus-encoded rna silencing suppressors, p14 ofbeet necrotic yellow vein virusand s6 ofrice black streak dwarf virus. CHINESE SCI BULL. 2005; 50: 305–310.

51. Supyani S, Hillman BI, Suzuki N. Baculovirus expression of the 11 mycoreovirus-1 genome segments and identification of the guanylyltransferase-encoding segment. J Gen Virol. 2007; 88: 342–50. doi: 10.1099/vir.0.82318-0 17170467

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