Anastomosis group and pathogenicity of Rhizoctonia spp. associated with seedling damping-off of sugar beet in China

Abstract

Between 2010 and 2015, 204 Rhizoctonia isolates were obtained from diseased sugar beet seedlings which collected from the sugar beet growing regions of China. On the basis of the morphological characteristics and sequence analysis of the internal transcribed spacers of the ribosomal DNA (rDNA ITS), 166 were identified as multinucleate Rhizoctonia (MNR), and 38 were binucleate Rhizoctonia (BNR), belonging to 15 species, anastomosis groups (AGs) or subgroups. The most prevalent was Rhizoctonia solani AG-4, with 49 isolates attributed to the subgroup HGIII, 47 to HGII, and 45 to HGI, followed by AG-K (31), AG-2-2IIIB (7), AG-A (6), AG-1-1C (4), AG-1-1B (3), AG-2-1 (3), AG-5 (3), AG-11 (2), AG-3 TB (1), Waitea circinata var. circinata (1), W. circinata var. zeae (1), and AG-C (1). Seventy-four representative isolates of all species, AGs or subgroups from different geographic origins were able to cause brown, dry lesions on roots of sugar beet seedlings or even seedling death with the disease incidence and the disease index ranging from 13.3 to 100% and from 1.9 to 97.1, respectively. The AG-4 isolates were the most aggressive on sugar beet seedlings. Moreover, the aggressiveness of the R. solani isolates was higher than that of the other isolates. To the best of our knowledge, this is the first detailed description of the AG composition of Rhizoctonia causing seedling damping-off on sugar beet in China.

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

Fig. 1
Fig. 2

References

  1. Ahvenniemi, P., Wolf, M., Lehtonen, M. J., Wilson, P., German-kinnari, M., & Valkonen, J. P. (2009). Evolutionary diversification indicated by compensatory base changes in ITS2 secondary structures in a complex fungal species, Rhizoctonia solani. Journal of Molecular Evolution, 69(2), 150–163.

    CAS  PubMed  Article  Google Scholar 

  2. Ajayi-Oyetunde, O. O., & Bradley, C. A. (2017). Identification and characterization of Rhizoctonia species associated with soybean seedling disease. Plant Disease, 101(4), 520–533.

    PubMed  Article  Google Scholar 

  3. Bacharis, C., Gouziotis, A., Kalogeropoulou, P., Koutita, O., Tzavella-Klonari, K., & Karaoglanidis, G. (2010). Characterization of Rhizoctonia spp. isolates associated with damping-off disease in cotton and tobacco seedlings in Greece. Plant Disease, 94(11), 1314–1322.

    CAS  PubMed  Article  Google Scholar 

  4. Berdugo, C., Hillnhütter, C., Sikora, R., & Oerke, E. C. (2012). A resistance bioassay for Rhizoctonia root and crown rot and damping-off caused by the anastomosis groups AG-2-2IIIB and AG-4 in sugar beet. Journal of Agricultural Science and Technology, A2(3), 294–302.

    Google Scholar 

  5. Carling, D. E. (1996). Grouping in Rhizoctonia solani by the anastomosis reaction. In B. Sneh, S. Jabaji-Hare, S. Neate, & G. Dijst (Eds.), Rhizoctonia species: Taxonomy, molecularbiology, ecology, pathology and disease control (pp. 37–47). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  6. Carling, D., Kuninaga, S., & Brainard, K. (2002). Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology, 92(1), 43–50.

    CAS  PubMed  Article  Google Scholar 

  7. de la Cerda, K. A., Douhan, G. W., & Wong, F. P. (2007). Discovery and characterization of Waitea circinata var. circinata affecting annual bluegrass from the western United States. Plant Disease, 91(7), 791–797.

    PubMed  Article  CAS  Google Scholar 

  8. Dong, W. H., Li, Y. Q., Duan, C. F., Li, X. G., Naito, S., Conner, R. L., et al. (2017). Identification of AG-V, a new anastomosis group of binucleate Rhizoctonia spp. from taro and ginger in Yunnan province. European Journal of Plant Pathology, 148(4), 895–906.

    Article  Google Scholar 

  9. Escande, A. R., & Echandi, E. (1991). Protection of potato from Rhizoctonia canker with binucleate Rhizoctonia fungi. Plant Pathology, 40(2), 197–202.

    Article  Google Scholar 

  10. Fang, X., Finnegan, P. M., & Barbetti, M. J. (2013). Wide variation in virulence and genetic diversity of binucleate Rhizoctonia isolates associated with root rot of strawberry in Western Australia. PLoS One, 8(2), e55877.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. García, V. G., Onco, M. P., & Susan, V. R. (2006). Biology and systematics of the form genus Rhizoctonia. Spanish Journal of Agricultural Research, 4(1), 55–79.

    Article  Google Scholar 

  12. Hall, G. (1986). A species of Rhizoctonia, with uninucleate hyphae isolated from roots of winter wheat. Transactions of the British Mycological Society, 87(3), 466–471.

    Article  Google Scholar 

  13. Hanson, L. E., & McGrath, J. M. (2010). Sugar beet seedling damping-off in Michigan. Phytopathology, 100(6S), S47.

    Google Scholar 

  14. Hanson, L. E., & McGrath, J. M. (2011). Rhizoctonia seedling disease on sugar beet. International Sugar Journal, 113(8), 584–589.

    Google Scholar 

  15. Harris, A. (2000). Solid formulations of binucleate Rhizoctonia isolates suppress Rhizoctonia solani and Pythium ultimum in potting medium. Microbiological Research, 154(4), 333–337.

    CAS  PubMed  Article  Google Scholar 

  16. Harveson, R. M., Hanson, L. E., & Hein, G. L. (2009). Compendium of beet diseases and pests. Ed. 2. American Phytopathological society. (APS press) 21–24.

  17. Hayakawa, T., Toda, T., Ping, Q., Mghalu, J. M., Yaguchi, S., & Hyakumachi, M. (2006). A new subgroup of Rhizoctonia AG-D, AG-D III, obtained from Japanese zoysia grass exhibiting symptoms of a new disease. Plant Disease, 90(11), 1389–1394.

    CAS  PubMed  Article  Google Scholar 

  18. Hietala, A. M. (1995). Uni-and binucleate Rhizoctonia spp. co-existing on the roots of Norway-spruce seedlings suffering from root dieback. Forest Pathology, 25(3), 136–144.

    Article  Google Scholar 

  19. Hietala, A. M., Vahala, J., & Hantula, J. (2001). Molecular evidence suggests that Ceratobasidium bicorne has an anamorph known as a conifer pathogen. Mycological Research, 105(5), 555–562.

    CAS  Article  Google Scholar 

  20. Kuramae, E. E., Buzeto, A. L., Ciampi, M. B., & Souza, N. L. (2003). Identification of Rhizoctonia solani AG 1-IB in lettuce, AG 4 HG-I in tomato and melon, and AG 4 HG-III in broccoli and spinach, in Brazil. European Journal of Plant Pathology, 109(4), 391–395.

    CAS  Article  Google Scholar 

  21. Kuznia, R., & Windels, C. (1994). Rhizoctonia zeae pathogenic to spring wheat and sugar beet seedlings. Phytopathology, 84(10), 1159.

    Google Scholar 

  22. Li, J., Xia, H. B., & Yu, J. F. (2011). The anastomosis groups of the corn sheath blight pathogen Rhizoctonia spp. in northeastern China. Mycosystema, 30(3), 392–399 (in Chinese).

    CAS  Google Scholar 

  23. Lilja, A., Hietala, A. M., & Karjalainen, R. (1996). Identification of a uninucleate Rhizoctonia spp. by pathogenicity, hyphal anastomosis and RAPD analysis. Plant Pathology, 45(5), 997–1006.

    CAS  Article  Google Scholar 

  24. Nagendran, S., Hammerschmidt, R., & McGrath, J. M. (2009). Identification of sugar beet germplasm EL51 as a source of resistance to post-emergence Rhizoctonia damping-off. European Journal of Plant Pathology, 123(4), 461–471.

    Article  Google Scholar 

  25. Nelson, B., Helms, T., Christianson, T., & Kural, I. (1996). Characterization and pathogenicity of Rhizoctonia from soybean. Plant Disease, 80(1), 74–80.

    Article  Google Scholar 

  26. Ogoshi, A. (1987). Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kuhn. Annual Review of Phytopathology, 25(1), 125–143.

    Article  Google Scholar 

  27. O'sullivan, E., & Kavanagh, J. (1991). Characteristics and pathogenicity of isolates of Rhizoctonia spp. associated with damping-off of sugar beet. Plant Pathology, 40(1), 128–135.

    Article  Google Scholar 

  28. Otero, J. T., Ackerman, J. D., & Bayman, P. (2002). Diversity and host specificity of endophytic Rhizoctonia-like fungi from tropical orchids. American Journal of Botany, 89(11), 1853–1858.

    Article  Google Scholar 

  29. Priyatmojo, A., Yamauchi, R., Kageyama, K., & Hyakumachi, M. (2001). Grouping of binucleate Rhizoctonia anastomosis group D (AG-D) isolates into subgroups I and II based on whole-cell fatty acid compositions. Journal of Phytopathology, 149(7–8), 421–426.

    CAS  Article  Google Scholar 

  30. Sharon, M., Freeman, S., Kuninaga, S., & Sneh, B. (2007). Genetic diversity, anastomosis groups and virulence of Rhizoctonia spp. from strawberry. European Journal of Plant Pathology, 117(3), 247–265.

    CAS  Article  Google Scholar 

  31. Sharon, M., Sneh, B., Kuninaga, S., Hyakumachi, M., & Naito, S. (2008). Classification of Rhizoctonia spp. using rDNA ITS sequence analysis supports the genetic basis of the classical anastomosis grouping. Mycoscience, 49(2), 93–114.

    CAS  Article  Google Scholar 

  32. Smiley, R., & Uddin, W. (1993). Influence of soil temperature on Rhizoctonia root rot (R. solani AG-8 and R. oryzae) of winter wheat. Phytopathology, 83(9), 777–785.

    Article  Google Scholar 

  33. Soltaninezhad, S., Mahmoudi, S. B., & Farokhi, N. R. (2008). Characterization of sugar beet Rhizoctonia isolates in Iran. Journal of Sugar Beet, 23(2), 135–150.

    Google Scholar 

  34. Strausbaugh, C. A., Eujayl, I. A., Panella, L. W., & Hanson, L. E. (2011). Virulence, distribution and diversity of Rhizoctonia solani from sugar beet in Idaho and Oregon. Canadian Journal of Plant Pathology, 33(2), 210–226.

    Article  Google Scholar 

  35. Taheri, P., & Tarighi, S. (2012). Genetic and virulence analysis of Rhizoctonia spp. associated with sugar beet root and crown rot in the northeast region of Iran. Plant Disease, 96(3), 398–408.

    PubMed  Article  Google Scholar 

  36. Taheri, P., Gnanamanickam, S., & Höfte, M. (2007). Characterization, genetic structure, and pathogenicity of Rhizoctonia spp. associated with rice sheath diseases in India. Phytopathology, 97(3), 373–383.

    CAS  PubMed  Article  Google Scholar 

  37. Toda, T., Mushika, T., Hayakawa, T., Tanaka, A., Tani, T., & Hyakumachi, M. (2005). Brown ring patch: A new disease on bentgrass caused by Waitea circinata var. circinata. Plant Disease, 89(6), 536–542.

    CAS  PubMed  Article  Google Scholar 

  38. Wang, P. P., & Wu, X. H. (2012). First report of sugar beet seedling damping-off caused by binucleate Rhizoctonia AG-A in China. Plant Disease, 96(11), 1696.

    CAS  PubMed  Article  Google Scholar 

  39. Webb, K. M., Hill, A. L., Laufman, J., Hanson, L. E., & Panella, L. (2011). Long-term preservation of a collection of Rhizoctonia solani using cryogenic storage. Annals of Applied Biology, 158(3), 297–304.

    Article  Google Scholar 

  40. White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

  41. Windeis, С., & Nabben, D. J. (1989). Characterization and pathogenicity of anastomosis groups of Rhizoctonia solani isolated from Beta vulgaris. Phytopathology, 79(1), 83–88.

    Article  Google Scholar 

  42. Yang, G. H., Chen, H. R., Naito, S. Y., Ogoshi, A., & Deng, Y. L. (2005). First report of AG-A of binucleate Rhizoctonia in China, pathogenic to soya bean, pea, snap bean and pak choy. Journal of Phytopathology, 153(6), 333–336.

    CAS  Article  Google Scholar 

  43. Yang, Y. G., Zhao, C., Guo, Z. J., & Wu, X. H. (2014). Anastomosis groups and pathogenicity of binucleate Rhizoctonia isolates associated with stem canker of potato in China. European Journal of Plant Pathology, 139(3), 535–544.

    CAS  Article  Google Scholar 

  44. Yang, Y. G., Zhao, C., Guo, Z. J., & Wu, X. H. (2015a). Anastomosis group and pathogenicity of Rhizoctonia solani associated with stem canker and black scurf of potato in China. European Journal of Plant Pathology, 143(1), 99–111.

    Article  Google Scholar 

  45. Yang, Y. G., Zhao, C., Guo, Z. J., & Wu, X. H. (2015b). Characterization of a new anastomosis group (AG-W) of binucleate Rhizoctonia, causal agent for potato stem canker. Plant Disease, 99(12), 1757–1763.

    CAS  PubMed  Article  Google Scholar 

  46. Zhao, C., & Wu, X. H. (2014). First report of sugar beet Rhizoctonia crown and root rot caused by Rhizoctonia solani AG-2-2IIIB in Shanxi province of China. Plant Disease, 98(3), 419.

    CAS  PubMed  Article  Google Scholar 

  47. Zhao, S. F., Li, G. Y., Li, H., & Wang, Q. Y. (2002). Identification of pathogen population of sugar beet root rot disease in Xinjiang. Sugar Crops of China, 1, 3–8 (in Chinese).

    Google Scholar 

  48. Zhou, S. Y., Zhang, M., Liu, Y., Zhen, J., Liang, W. X., Chen, X. J., et al. (2015). A uninucleate Rhizoctonia sp. from maize plant with ITS heterogeneity and hypersensitive to abiotic stresses. European Journal of Plant Pathology, 142(2), 397–401.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the earmarked fund for China Agriculture Research System (CARS-170304). Mention of trade names or commercial products in this report is solely for the purpose of providing specific information and does not imply recommendation or endorsement.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Xuehong Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal studies

This article does not contain any studies with human or animal subjects.

Electronic supplementary material

ESM 1

(DOC 269 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhao, C., Li, Y., Wu, S. et al. Anastomosis group and pathogenicity of Rhizoctonia spp. associated with seedling damping-off of sugar beet in China. Eur J Plant Pathol 153, 869–878 (2019). https://doi.org/10.1007/s10658-018-1603-8

Download citation

Keywords

  • Sugar beet
  • Rhizoctonia
  • Anastomosis group
  • Pathogenicity
  • Internal transcribed spacer
  • DNA sequencing