Abstract
We report the recovery of a 7068-nt viral sequence from the “viral fossils” embedded in the genome of Alhagi sparsifolia, a typical desert plant. Although the full viral genome remains to be completed, the putative genome structure, the deduced amino acids and phylogenetic analysis unambiguously demonstrate that this viral sequence represents a novel species of the genus Badnavirus. The putative virus is tentatively termed Alhagi bacilliform virus (ABV). Southern blotting and inverse polymerase chain reaction (PCR) data indicate that the ABV-related sequence is integrated into the A. sparsifolia genome, and probably does not give rise to functional episomal virus. Molecular evidence that the ABV sequence exists widely in A. sparsifolia is also presented. To our knowledge, this is the first endogenous badnavirus identified from plants in the Gobi desert, and may provide new clues on the evolution, geographical distribution as well as the host range of the badnaviruses.
概 要
目 的
新杆状 DNA 病毒的分离与鉴定。
创新点
首次在高寒地区代表性植物——疏叶骆驼刺中发现杆状 DNA 病毒, 为研究杆状 DNA 病毒的进化、 地理分布及寄主范围提供了新证据。
方 法
利用分段聚合酶链式反应 (PCR) 克隆疏叶骆驼刺杆状病毒 (Alhagi bacilliform virus, ABV) 的基因组序列; 通过基因组分析、 序列比对和进化树分析阐明 ABV 的进化地位; 用 Southern 印迹杂交和反向 PCR 分析 ABV 序列与宿主基因组的关系; 并通过 PCR 检测确定 ABV 在我国西北地区疏叶骆驼刺中的分布。
结 论
本研究获得了 7068 nt 的 ABV 基因组序列, 根据基因组结构、 保守序列比对及进化树分析, 推测 ABV 是一种新杆状 DNA 病毒。 分子检测证据表明, ABV 基因组序列已整合进入疏叶骆驼刺基因组中, 但没有产生游离病毒。 此外, 对我国西北 11 个不同地区的疏叶骆驼刺进行 PCR 检测, 结果显示其中 9 个地区的疏叶骆驼刺均含有 ABV 序列, 由此表明 ABV 在我国西北地区的疏叶骆驼刺中广泛存在。
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References
Bhat AI, Hohn T, Selvarajan R, 2016. Badnaviruses: the current global scenario. Viruses, 8(6):177. https://doi.org/10.3390/v8060177.
Chabannes M, Baurens FC, Duroy PO, et al., 2013. Three infectious viral species lying in wait in the banana genome. J Virol, 87(15):8624–8637. https://doi.org/10.1128/JVI.00899-13.
Cheng CP, Lockhart BEL, Olszewski NE, 1996. The ORF I and II proteins of Commelina yellow mottle virus are virion-associated. Virology, 223(2):263–271. https://doi.org/10.1006/viro.1996.0478.
Fauquet CM, Mayo MA, Maniloff J, et al., 2005. Virus taxonomy, classification and nomenclature of viruses. Eighth Report of the International Committee on the Taxonomy of Viruses. Elsevier Academic Press, San Diego.
Feschotte C, Gilbert C, 2012. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet, 13(4):283–296. https://doi.org/10.1038/nrg3199.
Gawel NJ, Jarret RL, 1991. A modified CTAB DNA extraction procedure for Musa and Ipomoea. Plant Mol Biol Rep, 9(3):262–266. https://doi.org/10.1007/BF02672076.
Gayral P, Noa-Carrazana JC, Lescot M, et al., 2008. A single Banana streak virus integration event in the banana genome as the origin of infectious endogenous pararetrovirus. J Virol, 82(13):6697–6710. https://doi.org/10.1128/JVI.00212-08.
Geering ADW, Olszewski NE, Dahal G, et al., 2001. Analysis of the distribution and structure of integrated Banana streak virus DNA in a range of Musa cultivars. Mol Plant Pathol, 2(4):207–213. https://doi.org/10.1046/j.1464-6722.2001.00071.x.
Geering ADW, Olszewski NE, Harper G, et al., 2005a. Banana contains a diverse array of endogenous badnaviruses. J Gen Virol, 86(2):511–520. https://doi.org/10.1099/vir.0.80261-0.
Geering ADW, Pooggin MM, Olszewski NE, et al., 2005b. Characterisation of Banana streak Mysore virus and evidence that its DNA is integrated in the B genome of cultivated Musa. Arch Virol, 150(4):787–796. https://doi.org/10.1007/s00705-004-0471-z.
Geijskes RJ, Braithwaite KS, Dale JL, et al., 2002. Sequence analysis of an Australian isolate of Sugarcane bacilliform badnavirus. Arch Virol, 147(12):2393–2404. https://doi.org/10.1007/s00705-002-0879-2.
Gregor W, Mette MF, Staginnus C, et al., 2004. A distinct endogenous pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol, 134(3):1191–1199. https://doi.org/10.1104/pp.103.031112.
Hansen CN, Harper G, Heslop-Harrison JS, 2005. Characterisation of pararetrovirus-like sequences in the genome of potato (Solanum tuberosum). Cytogenet Genome Res, 110(1-4):559–565. https://doi.org/10.1159/000084989.
Hany U, Adams IP, Glover R, et al., 2014. The complete genome sequence of Piper yellow mottle virus (PYMoV). Arch Virol, 159(2):385–388. https://doi.org/10.1007/s00705-013-1824-2.
Harper G, Hull R, Lockhart B, et al., 2002. Viral sequences integrated into plant genomes. Ann Rev Phytopathol, 40(1):119–136. https://doi.org/10.1146/annurev.phyto.40.120301.105642.
Harper G, Hart D, Moult S, et al., 2004. Banana streak virus is very diverse in Uganda. Virus Res, 100(1):51–56. https://doi.org/10.1016/j.virusres.2003.12.024.
Hohn T, Fütterer J, Hull R, 1997. The Proteins and functions of plant pararetroviruses: knowns and unknowns. Crit Rev Plant Sci, 16(1):133–161. https://doi.org/10.1080/713608145.
Hull R, Harper G, Lockhart B, 2000. Viral sequences integrated into plant genomes. Trends Plant Sci, 5(9):362–365. https://doi.org/10.1016/S1360-1385(00)01723-4.
Iskra-Caruana ML, Duroy PO, Chabannes M, et al., 2014. The common evolutionary history of badnaviruses and banana. Infect Genet Evol, 21:83–89. https://doi.org/10.1016/j.meegid.2013.10.013.
Jacquot E, Hagen LS, Jacquemond M, et al., 1996. The open reading frame 2 product of cacao swollen shoot badnavirus is a nucleic acid-binding protein. Virology, 225(1): 191–195. https://doi.org/10.1006/viro.1996.0587.
Kazmi SA, Yang Z, Hong N, et al., 2015. Characterization by small RNA sequencing of Taro bacilliform CH virus (TaBCHV), a novel badnavirus. PLoS ONE, 10(7): e0134147. https://doi.org/10.1371/journal.pone.0134147.
King AMQ, Adams MJ, Lefkowitz EJ, et al., 2012. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA, USA.
Laney AG, Hassan M, Tzanetakis IE, 2012. An integrated badnavirus is prevalent in fig germplasm. Phytopathology, 102(12):1182–1189. https://doi.org/10.1094/PHYTO-12-11-0351.
Medberry SL, Lockhart BE, Olszewski NE, 1990. Properties of Commelina yellow mottle virus’s complete DNA sequence, genomic discontinuities and transcript suggest that it is a pararetrovirus. Nucleic Acids Res, 18(18): 5505–5513. https://doi.org/10.1093/nar/18.18.5505.
Philippe G, Marie I, 2009. Phylogeny of Banana streak virus reveals recent and repetitive endogenization in the genome of its banana host (Musa sp.). J Mol Evol, 69(1): 65–80. https://doi.org/10.1007/s00239-009-9253-2.
Seal S, Muller E, 2007. Molecular analysis of a full-length sequence of a new yam badnavirus from Dioscorea sansibarensis. Arch Virol, 152(4):819–825. https://doi.org/10.1007/s00705-006-0888-7.
Seal S, Turaki A, Muller E, et al., 2014. The prevalence of badnaviruses in West African yams (Dioscorea cayenensisrotundata) and evidence of endogenous pararetrovirus sequences in their genomes. Virus Res, 186:144–154. https://doi.org/10.1016/j.virusres.2014.01.007.
Staginnus C, Richert-Pöggeler KR, 2006. Endogenous pararetroviruses: two-faced travelers in the plant genome. Trends Plant Sci, 11(10):485–491. https://doi.org/10.1016/j.tplants.2006.08.008.
Su L, Gao S, Huang Y, et al., 2007. Complete genomic sequence of Dracaena mottle virus, a distinct badnavirus. Virus Genes, 35(2):423–429. https://doi.org/10.1007/s11262-007-0102-3.
Tamura K, Peterson D, Peterson N, et al., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol, 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121.
Tzafrir I, Ayala-Navarrete L, Lockhart BEL, et al., 1997. The N-terminal portion of the 216-kDa polyprotein of Commelina yellow mottle badnavirus is required for virus movement but not for replication. Virology, 232(2): 359–368. https://doi.org/10.1006/viro.1997.8569.
Umber M, Filloux D, Muller E, et al., 2014. The genome of African yam (Dioscorea cayenensis-rotundata complex) hosts endogenous sequences from four distinct badnavirus species. Mol Plant Pathol, 15(8):790–801. https://doi.org/10.1111/mpp.12137.
Wang Y, Cheng X, Wu X, et al., 2014. Characterization of complete genome and small RNA profile of pagoda yellow mosaic associated virus, a novel badnavirus in China. Virus Res, 188:103–108. https://doi.org/10.1016/j.virusres.2014.04.006.
Wu H, Zhang Y, Zhang W, et al., 2015. Transcriptomic analysis of the primary roots of Alhagi sparsifolia in response to water stress. PLoS ONE, 10(3):e0120791. https://doi.org/10.1371/journal.pone.0120791.
Xu D, Mock R, Kinard G, et al., 2011. Molecular analysis of the complete genomic sequences of four isolates of Gooseberry vein banding associated virus. Virus Genes, 43(1):130–137. https://doi.org/10.1007/s11262-011-0614-8.
Yang IC, Hafner GJ, Dale JL, et al., 2003. Genomic characterisation of Taro bacilliform virus. Arch Virol, 148(5): 937–949. https://doi.org/10.1007/s00705-002-0969-1.
Yang Z, Nicolaisen M, Olszewski NE, et al., 2005. Sequencing, improved detection, and a novel form of Kalanchoë top-spotting virus. Plant Dis, 89(3):298–302. https://doi.org/10.1094/PD-89-0298
Acknowledgements
We thank Dr. Wang-bin ZHANG (College of Plant Science, Tarim University, the Xinjiang Uygur Autonomous Region, China) and Dr. Xin-wu PEI (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, China) for helping collect the seeds of A. sparsifolia, and Dr. Hong-yan SHAN (Institute of Botany, Chinese Academy of Sciences, Beijing, China) for her helpful suggestion to construct the phylogenetic trees.
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Project supported by the National Natural Science Foundation of China (Nos. 31370181 and 31570146) and the Fujian Natural Science Funds for Distinguished Young Scholar (No. 2014J06008), China
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Li, Yc., Shen, Jg., Zhao, Gh. et al. A novel endogenous badnavirus exists in Alhagi sparsifolia. J. Zhejiang Univ. Sci. B 19, 274–284 (2018). https://doi.org/10.1631/jzus.B1700171
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DOI: https://doi.org/10.1631/jzus.B1700171