Complete genome sequences and recombination analysis of three divergent Satsuma dwarf virus isolates


Citrus mosaic virus (CiMV) and navel orange infectious mottling virus (NIMV) are considered strains of satsuma dwarf virus (SDV). To understand the distribution of different isolates of SDV in China, a field survey was conducted, which allowed for the detection of CiMV and NIMV in citrus plants in Zhejiang and Sichuan provinces, respectively. In the present work, two CiMV isolates, including one named CiMV-GTC1 from Goutoucheng sour orange and one named CiMV-SE1 from Setoka tangor, as well as one NIMV isolate named NIMV-EH1 from Ehime-ken No. 38 tangor were, for the first time, fully sequenced. Among the isolates, CiMV-SE1 and CiMV-GTC1 were closely associated with the partial genomes of known CiMV isolates, while NIMV-EH1 was markedly different from known NIMV isolate. Sequence analysis demonstrated that CiMV, NIMV, and SDV shared similar genome organization and high nucleotide identities at the genome level. In addition, phylogenetic reconstruction of the three viruses also suggested a close relationship. Furthermore, recombination analysis provided evidence for their common co-occurrence in nature. These findings contribute significantly to our understanding of the natural evolution of SDV populations and can provide a basis for preventing the spread of different SDV isolates in the main citrus production regions.

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  1. Azeri T (1973) First report of Satsuma dwarf virus disease on Satsuma mandarins in Turkey. IEEE International Symposium on Circuits & Systems 57:149–153

  2. Cui PF, Gu CF, Roistacher CN (1991) Occurrence of Satsuma dwarf virus in Zhejiang Province, China. Plant Disease 75:242–244

  3. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Xian A, Fan L, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnology 29:644–652

  4. Ito T, Iwanami T, Ieki H, Shimomura K, Shimizu S (2004) A new virus related to Satsuma dwarf virus: the nucleotide sequence of the 3′-terminal regions of Hyuganatsu virus RNAs 1 and 2. Archives of Virology 149:1459–1465

  5. Ito T, Ito T, Shiotani H, Iwanami T, Ozaki K, Muramoto K (2007) Genetic diversity and a heterogeneous population of Citrus mosaic virus within a single citrus tree. Journal of General Plant Pathology 73:147–151

  6. Iwanami T (2010) Properties and control of Satsuma dwarf virus. Japan Agricultural Research 44:1–6

  7. Iwanami T, Kondo Y, Karasev AV (1999) Nucleotide sequences and taxonomy of Satsuma dwarf virus. Journal of General Virology 80:793–797

  8. Iwanami T, Kondo Y, Kobayashi M, Han SS, Karasev AV (2001) Sequence diversity and interrelationships among isolates of Satsuma dwarf-related viruses. Archives of Virology 146:807–813

  9. Kim D (2001) Study on the virus infection state of Cheju-do area and the culture of virus-free stock. Hortscience 36:601

    Google Scholar 

  10. Koizumi M, Kano T, Ieki H, Mae H (1988) China laurestine: a symptomless carrier of Satsuma dwarf virus which accelerates natural transmission in the fields. International Organization of Citrus Virologists Conference Proceedings (1957–2010) 10, 348–352

  11. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874

  12. Lee RF (2015) Control of virus diseases of citrus. In: Loebenstein G, Katis NI (eds) Advances in virus research. Elsevier Academic Press, London, pp 143–173

    Google Scholar 

  13. 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

  14. Nakazono-Nagaoka E, Takemoto S, Fujikawa T, Nakajima K, Uenishi H, Iwanami T (2014) Natural Satsuma dwarf virus infection of two woody plants, Daphniphyllum teijsmannii Zoll. ex Kurz. and Viburnum odoratissimum Ker-Gaul. Var. awabuki (K. Koch) Zabel near citrus fields. Japan Agricultural Research Quarterly 48:419–424

  15. Sanfaçon H, Dasgupta I, Fuchs M, Karasev AV, Petrzik K, Thompson JR, Tzanetakis I, van der Vlugt R, Wetzel T, Yoshikawa N (2020) Proposed revision of the family Secoviridae taxonomy to create three subgenera, “Satsumavirus”, “Stramovirus” and “Cholivirus”, in the genus Sadwavirus. Archives of Virology 165:527–533

  16. Shimizu S-i, Ito T, Miyoshi T, Tachibana Y, Ito T (2011) A broad spectrum, one-step RT-PCR to detect Satsuma dwarf virus variants using universal primers targeting both segmented RNAs 1 and 2. Journal of General Plant Pathology 77:326–330

  17. Thompson JR, Dasgupta I, Fuchs M, Iwanami T, Karasev AV, Petrzik K, Sanfaçon H, Tzanetakis I, van der Vlugt R, Wetzel T (2017) ICTV virus taxonomy profile: Secoviridae. Journal of General Virology 98:529–531

  18. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng JY, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nature Genetics 45:59–66

  19. Zhou C, Zhao X, Jiang Y (1993a) Goutoucheng – a new indicator plant for citrus mosaic virus. International Organization of Citrus Virologists Conference Proceedings (1957–2010) 12, 368–370

  20. Zhou C, Zhao X, Jiang Y, He X (1993b) The distribution of Satsuma dwarf virus (SDV) in China. Acta Phytophylacica Sinica 20:123–127

    Google Scholar 

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This research was supported by the National Key R&D Program of China (2019YFD1001800, 2017YFE0110900), Fundamental Research Funds for the Central Universities (XDJK2018AA002), Chongqing Research Program of Basic Research and Frontier Technology (cstc2017jcyjBX0016), Innovation Program for Chongqing’s Overseas Returnees (cx2019013), and 111 Project (B18044). We thank LetPub ( for its linguistic assistance during the preparation of this manuscript.

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All authors contributed to the study conception and design. Conceptualization: Song Zhang, Changyong Zhou and Mengji Cao; Methodology: Song Zhang and Mengji Cao; Formal analysis and investigation: Jianhong Yan, Song Zhang, and Jiaxing Wu; Writing - original draft preparation: Jianhong Yan, Song Zhang; Writing - review and editing: Song Zhang, Changyong Zhou and Mengji Cao; Funding acquisition: Changyong Zhou and Mengji Cao; Resources: Fangyun Yang; Supervision: Changyong Zhou and Mengji Cao.

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Correspondence to Changyong Zhou or Mengji Cao.

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Yan, J., Zhang, S., Wu, J. et al. Complete genome sequences and recombination analysis of three divergent Satsuma dwarf virus isolates. Trop. plant pathol. 46, 26–30 (2021).

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  • Citrus mosaic virus
  • High-throughput sequencing
  • Novel orange infectious mottling virus