Skip to main content
Log in

Molecular characterization and phylogenetic analysis of hop stunt viroid isolates from sweet cherry in China

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Hop stunt viroid (HSVd), a member of the family Pospiviroidae, infects a large number of plants and causes substantial economic losses. In this study, HSVd was detected in dappled fruits of sweet cherry and then molecularly characterized. We sequenced 164 cDNA clones from six sweet cherry cultivars in the Shandong Province of China and identified 23 HSVd sequence variants, which ranged in size between 293 and 303 nucleotides (nt) and shared 97~99% sequence identity with each other. Characterization of HSVd variants revealed that three were predominant in sweet cherry trees. Phylogenetic analysis showed that most of the HSVd variants isolated from sweet cherry were clustered within the plum-type group and that two variants were clustered with the recombinant P-C group, regardless of geographic origin. This study identified 23 HSVd variants and provided the molecular characterization of viroid infection (HSVd) in sweet cherry in China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amari, K., Gomez, G., Myrta, A., Di Terlizzi, B., & Pallás, V. (2001). The molecular characterization of 16 new sequence variants of Hop stunt viroid reveals the existence of invariable regions and a conserved hammerhead-like structure on the viroid molecule. Journal of General Virology, 82(4), 953–962.

    Article  CAS  PubMed  Google Scholar 

  • Amari, K., Ruiz, D., Gómez, G., Sánchez-Pina, M. A., Pallás, V., & Egea, J. (2007). An important new apricot disease in Spain is associated with Hop stunt viroid infection. European Journal of Plant Pathology, 118(2), 173–181.

    Article  Google Scholar 

  • Astruc, N., Marcos, J. F., Macquaire, G., Candresse, T., & Pallás, V. (1996). Studies on the diagnosis of hop stunt viroid in fruit trees: Identification of new hosts and application of a nucleic acid extraction procedure based on non-organic solvents. European Journal of Plant Pathology, 102(9), 837–846.

    Article  CAS  Google Scholar 

  • Canizares, M. C., Marcos, J. F., & Pallás, V. (1999). Molecular characterization of an almond isolate of hop stunt viroid (HSVd) and conditions for eliminating spurious hybridization in its diagnosis in almond samples. European Journal of Plant Pathology, 105(6), 553–558.

    Article  CAS  Google Scholar 

  • De Rijk, P., Wuyts, J., & De Wachter, R. (2003). RnaViz 2: An improved representation of RNA secondary structure. Bioinformatics, 19(2), 299–300.

    Article  PubMed  Google Scholar 

  • Di Serio, F., Flores, R., Verhoeven, J. T., Li, S. F., Pallás, V., Randles, J. W., Sano, T., Vidalakis, G., & Owens, R. A. (2014). Current status of viroid taxonomy. Archives of Virology, 59(12), 3467–3478.

    Article  CAS  Google Scholar 

  • Diener, T. O., Smith, D., Hammond, R., Albanese, G., La Rosa, R., & Davino, M. (1988). Citrus B viroid identified as a strain of hop stunt viroid. Plant Disease, 72, 691–693.

    Article  Google Scholar 

  • Ding, B. (2009). The biology of viroid-host interactions. Annual Review of Phytopathology, 47(1), 105–131.

    Article  CAS  PubMed  Google Scholar 

  • Elleuch, A., Hamdi, I., Ellouze, O., Ghrab, M., Fkahfakh, H., & Drira, N. (2013). Pistachio (Pistacia vera L.) is a new natural host of Hop stunt viroid. Virus Genes, 47(2), 330–337.

    Article  CAS  PubMed  Google Scholar 

  • Flores, R., Hernandez, C., de Alba, A. E. M., Daros, J. A., & Di Serio, F. (2005). Viroids and viroid-host interactions. Annual Review of Phytopathology, 43, 117–139.

    Article  CAS  PubMed  Google Scholar 

  • Flores, R., Gago-Zachert, S., Serra, P., Sanjuán, R., & Elena, S. F. (2014). Viroids: survivors from the RNA world? Annual Review of Microbiology, 68, 395–414.

    Article  CAS  PubMed  Google Scholar 

  • Gazel, M., Ulubaș, Ç., & Çağlayan, K. (2008). Detection of Hop Stunt Viroid in sweet and sour cherry trees in Turkey by RT-PCR. Acta Horticulturae, (795, 2), 955–958.

  • Guo, L., Liu, S., Wu, Z., Mu, L., Xiang, B., & Li, S. (2008). Hop stunt viroid (HSVd) newly reported from hop in Xinjiang, China. Plant Pathology, 57(4), 764.

    Article  Google Scholar 

  • Hataya, T., Tsushima, T., & Sano, T. (2017). Hop stunt viroid. In A. Hadidi, R. Flores, J. W. Randles, & P. Palukaitis (Eds.), Viroids and satellites (pp. 199–210). San Diego: Academic Press, Elsevier.

    Chapter  Google Scholar 

  • Jo, Y., Chu, H., Kim, H., Cho, J. K., Lian, S., Choi, H., Kim, S. M., Kim, S. L., Lee, B. C., & Cho, W. K. (2017). Comprehensive analysis of genomic variation of Hop stunt viroid. European Journal of Plant Pathology, 148(1), 119–127.

    Article  CAS  Google Scholar 

  • Kofalvi, S. A., Marcos, J. F., Canizares, M. C., Pallas, V., & Candresse, T. (1997). Hop stunt viroid (HSVd) sequence variants from Prunus species: Evidence for recombination between HSVd isolates. Journal of General Virology, 78(12), 3177–3186.

    Article  CAS  PubMed  Google Scholar 

  • Kovalskaya, N., & Hammond, R. W. (2014). Molecular biology of viroid-host interactions and disease control strategies. Plant Science, 228, 48–60.

    Article  CAS  PubMed  Google Scholar 

  • Lemmetty, A., Werkman, A. W., & Soukainen, M. (2011). First report of Hop stunt viroid in greenhouse cucumber in Finland. Plant Disease, 95(5), 615.

    Article  CAS  PubMed  Google Scholar 

  • Li, S. F., Guo, R., Tsuji, M., & Sano, T. (2006). Two grapevine viroids in China and the possible detection of a third. Plant Pathology, 55(4), 564.

    Article  Google Scholar 

  • Lin, C. Y., Wu, M. L., Shen, T. L., Yeh, H. H., & Hung, T. H. (2015). Multiplex detection, distribution, and genetic diversity of Hop stunt viroid and Citrus exocortis viroid infecting citrus in Taiwan. Virology Journal, 12, 11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mu, L. X., Wu, Y. H., & Li, S. F. (2009). First report of Hop stunt viroid from almond tree in China. Journal of Plant Pathology, 91(4), 112.

    Google Scholar 

  • Ohno, T., Takamatsu, N., Meshi, T., & Okada, Y. (1983). Hop stunt viroid: Molecular cloning and nucleotide sequence of the complete cDNA copy. Nucleic Acids Research, 11(18), 6185–6197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owens, R. A., Chen, W., Hu, Y., & Hsu, Y. H. (1995). Suppression of potato spindle tuber viroid replication and symptom expression by mutations which stabilize the pathogenicity domain. Virology, 208, 554–564.

    Article  CAS  PubMed  Google Scholar 

  • Owens, R. A., Steger, G., Hu, Y., Fels, A., Hammond, R. W., & Riesner, D. (1996). RNA structural features responsible for potato spindle tuber viroid pathogenicity. Virology, 222, 144–158.

    Article  CAS  PubMed  Google Scholar 

  • Rizza, S., Catara, A., Ma, X. F., & Deng, Z. (2007). Detection of multiple infections of Citrus exocortis viroid, Citrus viroid III, and Hop stunt viroid variants in Hunan Province, China. Plant Disease, 91(9), 1205.

    Article  CAS  PubMed  Google Scholar 

  • Rubio, M., Gómez, E. M., Martínez-Gómez, P., & Dicenta, F. (2016). Behaviour of apricot cultivars against Hop stunt viroid. Journal of Phytopathology, 164(3), 193–197.

    Article  Google Scholar 

  • Sano, T., & Ishiguro, A. (1998). Viability and pathogenicity of intersubgroup viroid chimeras suggest possible involvement of the terminal right region in replication. Virology, 240, 238–244.

    Article  CAS  PubMed  Google Scholar 

  • Sano, T., Uyeda, I., Shikata, E., Meshi, T., Ohno, T., & Okada, Y. (1985). A viroid-like RNA isolated from grapevine has high sequence homology with hop stunt viroid. Journal of General Virology, 66(2), 333–338.

    Article  CAS  Google Scholar 

  • Sano, T., Hataya, T., Terai, Y., & Shikata, E. (1989). Hop stunt viroid strains from dapple fruit disease of plum and peach in Japan. Journal of General Virology, 70(6), 1311–1319.

    Article  CAS  PubMed  Google Scholar 

  • Sano, T., Candresse, T., Hammond, R.W., Diener, T.O., & Owens R.A. (1992). Identification of multiple structural domain regulating viroid pathogenicity. Proceedings of the National Academy of Sciences of the United States of America, 89, 10104–10108.

  • Semancik, J. S., Roistacher, C. N., Rivera-Bustamante, R., & Duran-Vila, N. (1988). Citrus cachexia viroid, a new viroid of citrus: Relationship to viroids of the exocortis disease complex. Journal of General Virology, 69, 3059–3068.

    Article  Google Scholar 

  • Shikata, E. (1990). New viroids fron Japan. Seminars of Virology, I, 107–115.

    Google Scholar 

  • Wang, X. F., Zhou, Y., Li, Z. G., Tang, K. Z., Liu, Y. Q., Cao, M. J., & Zhou, C. Y. (2010). Molecular, biological and phylogenetic analysis of Chinese isolates of Hop stunt viroid associated with citrus cachexia disease. Journal of Phytopathology, 158, 372–377.

    Article  CAS  Google Scholar 

  • Xu, L., Wang, J. W., Zhu, D. Z., Zong, X. J., Wei, H. R., Chen, X., Hammond, R. W., & Liu, Q. Z. (2017). First report of Hop stunt viroid from sweet cherry with dapple fruit symptoms in China. Plant Disease, 101(2), 394.

    Article  CAS  Google Scholar 

  • Yang, Y. A., Wang, H. Q., Guo, R., Cheng, Z. M., Li, S. F., & Sano, T. (2006). First report of Hop stunt viroid in apricot in China. Plant Disease, 90(6), 828.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y. A., Wang, H. Q., Cheng, Z. M., Sano, T., & Li, S. F. (2007). First report of Hop stunt viroid from plum in China. Plant Pathology, 56, 339.

    Article  Google Scholar 

  • Yang, Y. A., Wang, H. Q., Wu, Z. J., Cheng, Z. M., & Li, S. F. (2008). Molecular variability of Hop stunt viroid: Identification of a unique variant with a tandem 15-nucleotide repeat from naturally infected plum tree. Biochemical Genetics, 46(3–4), 113–123.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B. L., Liu, G. Y., Liu, C. Q., Wu, Z. J., Jiang, D. M., & Li, S. F. (2009). Characterisation of Hop stunt viroid (HSVd) isolates from jujube trees (Ziziphus jujuba). European Journal of Plant Pathology, 125(4), 665–669.

    Article  CAS  Google Scholar 

  • Zhou, Y., Guo, R., Cheng, Z., Sano, T., & Li, S. F. (2006). First report of Hop stunt viroid from Prunus persica with dapple fruit symptoms in China. Plant Pathology, 55(4), 564.

    Article  Google Scholar 

  • Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31(13), 3406–3415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by Research Funds for Youth of Shandong Academy of Agricultural Sciences (2016YQN25) and Special Found for Fruit Innovation Team of Shandong Modern Agricultural Technology System (SDAIT-06-04).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Rosemarie W. Hammond or Qingzhong Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and/or animals rights

We confirm that in this research any human and/or animals participant was not used and there is no any disagreement with informed consent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, L., Wang, J., Chen, X. et al. Molecular characterization and phylogenetic analysis of hop stunt viroid isolates from sweet cherry in China. Eur J Plant Pathol 154, 705–713 (2019). https://doi.org/10.1007/s10658-019-01693-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01693-3

Keywords

Navigation