Skip to main content
Log in

Group 16SrXII phytoplasma strains, including subgroup 16SrXII-E (‘Candidatus Phytoplasma fragariae’) and a new subgroup, 16SrXII-I, are associated with diseased potatoes (Solanum tuberosum) in the Yunnan and Inner Mongolia regions of China

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

Abstract

In China, potato is widely cultivated economic crop. Recently, potato diseases with characteristic symptoms of phytoplasma infections were found in potato fields. In 2006 and 2007, samples exhibiting symptoms including rosette and upright growth, upward rolling, yellowing and purpling of leaves, shortened and thickened internodes and formation of aerial tubers were collected from plants in Yunnan and Inner Mongolia and analyzed for the presence of phytoplasmas. DNA was extracted from tissues of 63 symptomatic and 10 asymptomatic plants. Phytoplasma 16S rRNA was amplified by PCR with primer pair P1/P7, followed by nested PCR with P1A/P7A, P1A/16S-SR or R16F2n/R16R2n. Twenty nine symptomatic plants (46 %), but no asymptomatic plants, tested positive for phytoplasmas. Nested PCR products were cloned and sequenced. Sequence analysis indicated that the phytoplasmas from diseased potatoes shared 98.1–99.8 % similarity with ‘Candidatus Phytoplasma fragariae’ (16SrXII-E) and other strains in 16SrXII subgroups. RFLP and phylogenetic analyses also indicated that phytoplasmas of group 16SrXII were associated with phytoplasma infected potatoes in China; these strains are most closely related to subgroup 16SrXII-E. Our results showed that five strains belonged to 16SrXII-E; 11 strains were designated as a new 16SrXII subgroup, 16SrXII-I; and subgroup affiliations of all others were not determined. The genetic diversity of the strains was corroborated by sequence analysis of ribosomal protein genes, the elongation factor Tu gene (tuf) and the pre-protein translocase membrane subunit gene (secY). The results illustrated the complexity and diversity of phytoplasmas associated with potatoes 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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bertaccini, A. (2007). Phytoplasma: diversity, taxonomy, and epidemiology. Frontiers in Bioscience, 12, 673–689.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, M., Dong, J., Laski, P. J., Zhang, Z., & McBeath, J. H. (2011a). Molecular characterization of Candidatus Phytoplasma Asteris associated with aster yellows diseased potatoes in China. Plant Disease, 95, 777.

    Article  Google Scholar 

  • Cheng, M., Dong, J., Zhang, Z., & McBeath, J. H. (2011b). First report of clover proliferation group phytoplasmas (16SrVI-A) associated with purple top disease potatoes (Solanum tuberosum L.) in China. Plant Disease, 95, 871.

    Article  Google Scholar 

  • Cheng, M., Dong, J., Zhang, Z., & McBeath, J. H. (2012). Molecular characterization of stolbur group subgroup E (16SrXII-E) phytoplasma associated with potato in China. Plant Disease, 96, 1372.

    Article  Google Scholar 

  • Crosslin, J. M., Hamlin, L. L., Buchman, J. L., et al. (2011). Transmission of potato purple top phytoplasma to potato tubers and daughter plant. American Journal of Potato Research, 88, 339–345.

    Article  Google Scholar 

  • Deng, S., & Hiruki, C. (1991). Amplification of 16S rRNA genes from culturable and non-culturable mollicutes. Journal Microbiology Methods, 14, 53–61.

    Article  CAS  Google Scholar 

  • Duduk, B., & Bertaccini, A. (2006). Corn with symptoms of reddening: new host of stolbur phytoplasma. Plant Disease, 90, 1313–1319.

    Article  CAS  Google Scholar 

  • Eroglu, S., Ozbek, H., & Sahin, F. (2010). First report of group 16SrXII phytoplasma causing stolbur disease in potato plants in the eastern and southern Anatolia regions of Turkey. Plant Disease, 94, 1374.

    Article  Google Scholar 

  • Filippin, L., Angelini, E., & Borgo, M. (2008). First identification of a phytoplasma infecting Cornus sanguine and Sambucus nigra. Plant Pathology, 57, 1175.

    Article  Google Scholar 

  • Girsova, N., Bottner, K. D., Mozhaeva, K. A., Kastalyeva, T. B., Owens, R. A., & Lee, I.-M. (2008). Molecular detection and identification of group 16SrI and 16SrXII phytoplasma associated with diseased potatoes in Russia. Plant Disease, 92, 654.

    Article  Google Scholar 

  • Gundersen, D. E., & Lee, I.-M. (1996). Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathology Mediterranea, 35, 144–151.

    CAS  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Window 85/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hosseini, P., Bahar, M., Madani, G., & Zirak, L. (2011). Molecular characterization of phytoplasma associated with potato purple top disease in Iran. Journal of Phytopathology, 159, 241–246.

    Article  Google Scholar 

  • Jansky, S. H., Lin, L. P., Xie, K. Y., Xie, C. H., & Spooner, D. M. (2009). Potato production and breeding in China. Potato Research, 52, 57–65.

    Article  Google Scholar 

  • Jomantiene, R., Zhao, Y., Lee, I. M., & Davis, R. E. (2011). Phytoplasmas infecting sour cherry and lilac represent two distinct lineages having close evolutionary affinities with clover phyllody phytoplasma. European Journal of Plant Pathology, 130, 97–107.

    Article  CAS  Google Scholar 

  • Langer, M., & Maixner, M. (2004). Molecular characterization of grapevine yellows associated phytoplasmas of the stolbur-group based on PFLP-analysis of non-ribosomal DNA. Vitis, 43, 191–199.

    CAS  Google Scholar 

  • Laviña, L., & Batlle, A. (2002). First report of stolbur phytoplasma in avocado in Spain. Plant Disease, 86, 692.

    Article  Google Scholar 

  • Lee, I.-M., Gundersen-Rindal, D. E., Davis, R. E., & Bartoszyk, I. M. (1998). Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic Bacteriology, 48, 1153–1169.

    Article  CAS  Google Scholar 

  • Lee, I.-M., Davis, R. E., & Gundersen-Rindal, D. E. (2000). Phytoplasma: phytopathogenic mollicutes. Annual Review of Microbiology, 54, 221–255.

    Article  CAS  PubMed  Google Scholar 

  • Lee, I.-M., Martini, M., Marcone, C., & Zhu, S. F. (2004a). Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of ‘Candidatus phytoplasma ulmi’ for the phytoplasma associated with elm yellows. International Journal of Systematic and Evolutionary Microbiology, 54, 337–347.

    Article  CAS  PubMed  Google Scholar 

  • Lee, I,-M., Gundersen-Rindal, D. E., Davis, R.E., Bottner, K.D., Marcone, C., & Seemüller, E. (2004b). ‘Candidatus Phytoplasma asteris’, a novel phytoplasma taxon associated with aster yellows and related diseases. International Journal of Systematic and Evolutionary Microbiology, 54, 1037-1048.

  • Lee, I.-M., Bottner, K. D., Munyaneza, J. E., Davis, R. E., Crosslin, J. M., & du Toit, L. J. (2006a). Carrot purple leaf: a new spiroplasma disease associated with carrots in Washington State. Plant Disease, 90, 989–993.

    Article  CAS  Google Scholar 

  • Lee, I.-M., Bottner, K. D., Secor, G., & Rivera-Varas, V. (2006b). ‘Candidatus Phytoplasma americanum’, a phytoplasma associate with a potato purple top wilt disease complex. International Journal of Systematic and Evolutionary Microbiology, 56, 1593–1597.

    Article  CAS  PubMed  Google Scholar 

  • Lee, I.-M., Bottner, K. D., & Sun, M. (2009). An emerging potato purple top disease associated with a new 16SrIII group phytoplasma in Montana. Plant Disease, 93, 970.

    Article  Google Scholar 

  • Lee, I.-M., Bottner-Parker, K. D., Zhao, Y., Davis, R. E., & Harrison, N. A. (2010). Phylogenetic analysis and delineation of phytoplasmas based on secY gene sequences. International Journal of Systematic and Evolutionary Microbiology, 60, 2887–2897.

    Article  PubMed  Google Scholar 

  • Lee, I.-M., Zhao, Y., Suo, X., & Davis, R. E. (2011). Rapid and automated analysis of single nucleotide polymorphisms (SNPs) in secY gene sequences for finer differentiation and characterization of phytoplasmas. Bulletin of Insectology, 64(Supplement), S89–S90.

    Google Scholar 

  • Leyva-López, N. E., Ochoa-Sánchez, J. C., Leal-Klevezas, D. S., & Martinez-Soriano, J. P. (2002). Multiple phytoplasmas associated with potato diseases in Mexico. Canadian Journal of Microbiology, 48, 1062–1068.

    Article  PubMed  Google Scholar 

  • Liefting, L. W., Veerakone, S., Ward, L. I., & Clover, G. R. G. (2009). First report of ‘Candidatus phytoplasma australiense’ in potato. Plant Disease, 93, 969.

    Article  Google Scholar 

  • Liefting, L. W., Veerakone, S., & Clover, G. R. G. (2011). New hosts of ‘Candidatus Phytoplasma australiense’ in New Zealand. Australasian Plant Pathology, 40, 238–245.

    Article  Google Scholar 

  • Martini, M., Lee, I.-M., Bottner, K. D., Zhao, Y., Botti, S., Bertaccini, A., et al. (2007). Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. International Journal of Systematic and Evolutionary Microbiology, 57, 2037–2051.

    Article  CAS  PubMed  Google Scholar 

  • McBeath, J. H., & McBeath, J. (2010). Environmental change and food security in China. Dordrecht: Springer.

    Book  Google Scholar 

  • Paltrinieri, S., & Bertaccini, A. (2007). Detection of phytoplasma in plantlets grown from different batches of seed-potatoes. Bulletin of Insectology, 60, 379–380.

    Google Scholar 

  • Quaglino, F., Zhao, Y., Bianco, P. A., Wei, W., Casati, P., Durante, G., et al. (2009). New 16Sr subgroups and distinct single nucleotide polymorphism lineages among grapevine Bois noir phytoplasma populations. Annals of Applied Biology, 154, 279–289.

    Article  CAS  Google Scholar 

  • Santo-Cervantes, M. E., Chávez-Medina, J. A., Acosta-Pardini, J., Flores-Zamora, G. L., Méndez-Lozano, J., & Levva-López, N. E. (2010). Genetic diversity and geographical distribution of phytoplasmas associated with potato purple top disease in Mexico. Plant Disease, 94, 388–395.

    Article  Google Scholar 

  • Schneider, B., Seemüller, E., Smart, C. D., & Kirkpatrick, B. C. (1995). Phylogenetic classification of platn pathogenic mycoplasma-like organisms or phytoplasmas. In S. Razin & J. G. Tully (Eds.), Molecular and diagnostic procedures in mycoplasmology, vol. 2 (pp. 369–380). New York: Academic.

    Chapter  Google Scholar 

  • Schneider, B., Dudley, J., Nei, M., & Kumar, S. (1997). Sequence and RFLP analysis of the elongation factor Tu gene differentiation and classification of phytoplasms. Microbiology, 143, 3381–3389.

    Article  CAS  PubMed  Google Scholar 

  • Secor, G. A. (2007). The canon of plant science: 13. Phytoplasma diseases. Potato Research, 50, 255–257.

    Article  Google Scholar 

  • Tamura, K., Dudley, L., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  CAS  PubMed  Google Scholar 

  • Terlizzi, F., Babini, A. R., & Credo, R. (2006). First report of Stolbur phytoplasma (16SrXII-A) on strawberry in northern Italy. Plant Disease, 90, 831.

    Article  Google Scholar 

  • Untergrasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., & Leunissen, J. A. M. (2007). Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research, 35, W71–W73.

    Article  Google Scholar 

  • Valiunas, D., Staniulis, J., & Davis, R. E. (2006). ‘Candidatus Phytoplasma fragariae’, a novel phytoplasma taxon discovered in yellows diseased strawberry, Fragaria × ananassa. International Journal of Systematic and Evolutionary Microbiology, 56, 277–281.

    Article  CAS  PubMed  Google Scholar 

  • Wei, W., Davis, R. E., Lee, I.-M., & Zhao, Y. (2007). Computer-simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. International Journal of Systematic and Evolutionary Microbiology, 57, 1855–1867.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Cheng, M., Dong, J., et al. (2010). New potato disease associated withCandidatus Phytoplasma fragariaein China. Proceedings of the Annual Meeting of Chinese Society for Plant Protection.

  • Zhao, Y., Wei, W., Lee, I.-M., Shao, J., Suo, X., & Davis, R. E. (2009). Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). International Journal of Systematic and Evolutionary Microbiology, 59, 2582–2593.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by the USDA-FAS, Technical Assistance for Specialty Crops Program, the Yunnan Provincial Modern Agriculture for Potatoes Industrialization System ([2011]191), and Key Scientific and Technological Plan Project of Yunnan Province (2013ZA006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jenifer Huang McBeath.

Additional information

Mingyuan Cheng and Jiahong Dong contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Comparison of actual (top) and computer simulated virtual (bottom) RFLP patterns derived from digestion of R16F2n/R16R2n fragments (1.2 kb) of four 16SrXII phytoplasma strains from China with restriction enzymes AluI, HhaI, MseI, and TaqI. Lane M, ΦX174 RF DNA HaeIII digest, fragment sizes (bp) from top to bottom: 1,353, 1,078, 872, 603, 310, 281, 271, 234, 194, 118, 72. (PPTX 160 kb)

ESM 1

(XLSX 18 kb)

ESM 2

(DOCX 16 kb)

ESM 3

(XLSX 29 kb)

ESM 4

(XLSX 22 kb)

ESM 5

(XLSX 23 kb)

ESM 6

(XLSX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, M., Dong, J., Lee, IM. et al. Group 16SrXII phytoplasma strains, including subgroup 16SrXII-E (‘Candidatus Phytoplasma fragariae’) and a new subgroup, 16SrXII-I, are associated with diseased potatoes (Solanum tuberosum) in the Yunnan and Inner Mongolia regions of China. Eur J Plant Pathol 142, 305–318 (2015). https://doi.org/10.1007/s10658-015-0616-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0616-9

Keywords

Navigation