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Molecular characterization of a novel victorivirus isolated from Botryosphaeria dothidea, the causal agent of longan leaf spot disease

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Abstract

Mycoviruses are widespread in all major taxonomic groups of filamentous fungi. Previous research has indicated that mycoviruses are associated with the phytopathogenic fungus Botryosphaeria dothidea. In this study, three distinct double-stranded RNA viruses were detected in B. dothidea strain YCLYY11 isolated from a leaf spot of longan (Dimocarpus longana). The results of BLAST analysis revealed that the predicted amino acid sequences of those viruses were similar to those of Botryosphaeria dothidea chrysovirus 1, Botryosphaeria dothidea partitivirus 1, and an apparent novel victorivirus. Sequencing and analysis of the complete genome of the novel victorivirus indicated it is 5218 bp in length and contains two open reading frames (ORFs) that overlap at the tetranucleotide AUGA. BLASTp analysis of the proteins encoded by ORF1 and ORF2 showed that they were most similar to the coat protein and RNA-dependent RNA polymerase of Sphaeropsis sapinea RNA virus 2 (81.37% and 74.09% identical, respectively). A phylogenetic tree showed that the novel virus clustered together with victoriviruses and was separate from members of the other four genera of the family Totiviridae. Based on its genome structure and the results of phylogenetic analysis, we propose that this novel victorivirus should be named "Botryosphaeria dothidea victorivirus 3". This is also the first report of these three mycoviruses coinfecting a strain of B. dothidea.

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References

  1. Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479:356–368

    Article  Google Scholar 

  2. Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384

    Article  CAS  Google Scholar 

  3. Xie JT, Jiang DH (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68

    Article  CAS  Google Scholar 

  4. Liu LJ, Xie JT, Cheng JS, Fu YP, Li GQ, Yi XH, Jiang DH (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci USA 111:12205–12210

    Article  CAS  Google Scholar 

  5. Yu X, Li B, Fu YP, Jiang DH, Ghabrial SA, Li GQ, Peng YL, Xie JT, Cheng JS, Huang JB, Yi XH (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107(18):8387–8392

    Article  CAS  Google Scholar 

  6. Yu X, Li B, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci USA 110(4):1452–1457

    Article  CAS  Google Scholar 

  7. Tian B, Xie J, Fu Y, Cheng J, Li B, Chen T, Zhao Y, Gao Z, Yang P, Barbetti MJ, Tyler BM, Jiang D (2020) A cosmopolitan fungal pathogen of dicots adopts an endophytic lifestyle on cereal crops and protects them from major fungal diseases. ISME J 12:3120–3135

    Article  Google Scholar 

  8. Crous PW, Slippers B, Groenewald JZ, Wingfield MJ (2017) Botryosphaeriaceae: systematics, pathology, and genetics. Fungal Biol 121(4):305–306

    Article  Google Scholar 

  9. Marsberg A, Kemler M, Jami F, Nagel JH, Postma-Smidt A, Naidoo S, Wingfield MJ, Crous PW, Spatafora JW, Hesse CN, Robbertse B, Slippers B (2017) Botryosphaeria dothidea: a latent pathogen of global importance to woody plant health. Mol Plant Pathol 18:477–488

    Article  CAS  Google Scholar 

  10. Zhai L, Zhang M, Lv G, Chen X, Jia N, Hong N, Wang G (2014) Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis 98:716–726

    Article  Google Scholar 

  11. Wang L, Jiang J, Wang Y, Hong N, Zhang F, Xu W, Wang G (2014) Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus. J Virol 88(13):7517–7527

    Article  Google Scholar 

  12. Ding Z, Zhou T, Guo LY (2017) Characterization of a novel strain of Botryosphaeria dothidea chrysovirus 1 from the apple white rot pathogen Botryosphaeria dothidea. Arch Virol 162(7):2097–2102

    Article  CAS  Google Scholar 

  13. Yang M, Zhai L, Xiao F, Guo Y, Fu M, Hong N, Wang G (2019) Characterization of a novel victorivirus isolated from the phytopathogenic fungus Botryosphaeria dothidea. Arch Virol 164(6):1609–1617

    Article  CAS  Google Scholar 

  14. Zhai L, Hong N, Zhang M, Wang G (2015) Complete dsRNA sequence of a novel victorivirus isolated from the pear stem wart fungus Botryosphaeria dothidea. Arch Virol 160(2):613–616

    Article  CAS  Google Scholar 

  15. Zhai L, Yang M, Zhang M, Hong N, Wang G (2019) Characterization of a botybirnavirus conferring hypovirulence in the phytopathogenic fungus Botryosphaeria dothidea. Viruses 11(3):266

    Article  CAS  Google Scholar 

  16. Liu H, Liu M, Zhu H, Zhong J, Liao X, Zhou Q (2020) Molecular characterization of a novel mitovirus from the plant-pathogenic fungus Botryosphaeria dothidea. Arch Virol 166(2):633–637

    Article  Google Scholar 

  17. Wang H, Liu H, Lu X, Wang Y, Zhou Q (2021) A novel mitovirus isolated from the phytopathogenic fungus Botryosphaeria dothidea. Arch Virol 166(5):1507–1511

    Article  CAS  Google Scholar 

  18. Zhai L, Xiang J, Zhang M, Fu M, Yang Z, Hong N, Wang G (2016) Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology 493:75–85

    Article  CAS  Google Scholar 

  19. Liu H, Wang H, Zhou Q (2021) A novel mycovirus isolated from the plant-pathogenic fungus Botryosphaeria dothidea. Arch Virol 166(4):1267–1272

    CAS  PubMed  Google Scholar 

  20. Liu W, Hai D, Mu F, Yu X, Zhao Y, He B, Xie J, Jiang D, Liu H (2020) Molecular characterization of a novel fusarivirus infecting the plant-pathogenic fungus Botryosphaeria dothidea. Arch Virol 165(4):1033–1037

    Article  CAS  Google Scholar 

  21. Yang M, Zhou X, Zhai L, Xiao F, Hong N, Wang G (2020) Molecular characterization of a novel mycovirus infecting the phytopathogenic fungus Botryosphaeria dothidea. Arch Virol 165(7):1667–1670

    Article  CAS  Google Scholar 

  22. Yang M, Xu W, Zhou X, Yang Z, Wang Y, Xiao F, Guo Y, Hong N, Wang G (2021) Discovery and characterization of a novel bipartite botrexvirus from the phytopathogenic fungus Botryosphaeria dothidea. Front Microbiol 12:696125

    Article  Google Scholar 

  23. Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  24. Lambden PR, Cooke SJ, Caul EO, Clarke IN (1992) Cloning of noncultivatable human rotavirus by single primer amplification. J Virol 66:1817–1822

    Article  CAS  Google Scholar 

  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  26. Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166

    Article  CAS  Google Scholar 

  27. Preisig O, Wingfield BD, Wingfield MJ (1998) Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology 252(2):399–406

    Article  CAS  Google Scholar 

  28. Thapa V, Roossinck MJ (2019) Determinants of coinfection in the mycoviruses. Front Cell Infect Microbiol 9:169

    Article  CAS  Google Scholar 

  29. Khan HA, Shamsi W, Jamal A, Javaied M, Sadiq M, Fatma T, Ahmed A, Arshad M, Waseem M, Babar S, Dogar MM, Virk N, Janjua HA, Kondo H, Suzuki N, Bhatti MF (2021) Assessment of mycoviral diversity in Pakistani fungal isolates revealed infection by 11 novel viruses of a single strain of Fusarium mangiferae isolate SP1. J Gen Virol 102(12):001690

    Article  CAS  Google Scholar 

  30. Ghabrial SA, Nibert ML (2009) Victorivirus, a new genus of fungal viruses in the family Totiviridae. Arch Virol 154:37

    Article  Google Scholar 

  31. Li H, HavensWM NML, Ghabrial SA (2011) RNA sequence determinants of a coupled termination-reinitiation strategy for downstream open reading frame translation in Helminthosporium victoriae virus 190S and other victoriviruses (family Totiviridae). J Virol 85:7343–7352

    Article  CAS  Google Scholar 

  32. Li H, Havens WM, Nibert ML, Ghabrial SA (2015) An RNA cassette from Helminthosporium victoriae virus 190S necessary and sufficient for stop/restart translation. Virology 474:131–143

    Article  CAS  Google Scholar 

  33. Routhier E, Bruenn JA (1998) Functions of conserved motifs in the RNA-dependent RNA polymerase of a yeast double-stranded RNA virus. J Virol 72(5):4427–4429

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (32072476), the Natural Science Research Project of Chongqing Science and Technology (cstc2019jcyj-msxmX0200), the Science and Technology Research Program of Chongqing Municipal Education Commission (KJQN202001411, KJQN202001441), the  China Litchi and Longan Industry Technology Research System (CARS-32), and the Research Funding Project of Yangtze Normal University (2017KYQD54). We also thank Dr. Mengmeng Yang (Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou, China) for providing data from deep sequencing used for confirming the name of BdVV3. The authors thank AiMi Academic Services (www.aimieditor.com) for the English language editing and review services.

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Authors and Affiliations

  1. College of Biology and Food Engineering, Chongqing Three Gorges University, Chongqing, 404100, People’s Republic of China

    Jiali Li, Lifeng Zhai & Ming Liu

  2. College of Life Science and Biotechnology, Yangtze Normal University, Chongqing, 408100, People’s Republic of China

    Lifeng Zhai, Meixin Zhang, Gangjun Luo, Yongqi Wen, Tingting Cao, Huan Xia & Jiayu Zhang

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  1. Jiali Li
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Correspondence to Lifeng Zhai.

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Li, J., Zhai, L., Zhang, M. et al. Molecular characterization of a novel victorivirus isolated from Botryosphaeria dothidea, the causal agent of longan leaf spot disease. Arch Virol 167, 2417–2422 (2022). https://doi.org/10.1007/s00705-022-05573-w

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