Skip to main content
SpringerLink
Log in

Hypothesized mechanism of biocontrol against pine wilt disease by the nematophagous fungus Esteya vermicola

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

Abstract

Esteya vermicola is an endophytic fungus of pine wood nematode(s) (PWN) Bursaphelenchus xylophilus and a promising biocontrol agent. However, until now, only the lunate spores of E. vermicola have been demonstrated to be highly effective against pine wilt disease. In the present study, blastospores of E. vermicola were successfully used as a biocontrol agent through injection into large pine trees in Aewol-eup, Jeju, South Korea. When pine trees were injected with a 6–8 mL blastospore suspension of E. vermicola (108 mL−1) 1 month before inoculating them with PWN, 73.77% of the trees remained alive after one year. When injected with blastospores of E. vermicola 2 and 4 weeks after PWN infection, 40% of the trees were saved. As a control, the pine trees inoculated with PWN only all died. Moreover, a hypothesis of the mechanism of biocontrol within the pine tree was proposed based on the population density of PWN over time along with the presence of E. vermicola in the pine tree. The hypothesis involved a cycle that included the growth of E. vermicola without PWN infection, attraction and adhesion to PWN, movement and death of infected PWN, production of a second generation of lunate spores, and attraction of other migratory PWN.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aćimović, S. G., McGhee, G. C., Sundin, G. W., & Wise, J. C. (2015a). Control of fire blight (Erwinia amylovora) on apple trees with trunk-injected plant resistance inducers and antibiotics and assessment of induction of pathogenesis-related protein genes. Frontiers in Plant Science, 6, 16.

    PubMed  PubMed Central  Google Scholar 

  • Aćimović, S. G., McGhee, G. C., Sundin, G. W., & Wise, J. C. (2015b). Evaluation of trunk-injected bactericides and prohexadione-calcium for Environmentally friendly control of fire blight (Erwinia amylovora) in apples. Proceedings of the VII Congress on Plant Protection: Integrated Plant Protection–a Knowledge-Based Step towards Sustainable Agriculture, Forestry and Landscape Architecture 2014.

  • Baermann, G. (1917). Eine einfache methode zur auffindung von Ancylostomum (Nematoden) larven in erdproben. Geneeskd Tijdschr Ned Indie, 57, 131–137.

    Google Scholar 

  • Bick, E. N., Haugen, C., Bernick, S., & Herms, D. A. (2017). Efficacy of soil and trunk applied systemic insecticides for three years after application for control of emerald ash borer (Coleoptera: Buprestidae) on green ash. Arthropod Management Tests, 42(1), tsw134.

    Article  Google Scholar 

  • Davis, M. J., & Elkinton, J. S. (2018). Efficacy of two systemic insecticides with stem gall wasp, Zapatella davisae (Hymenoptera: Cynipidae) on black oak. Journal of Economic Entomology, 111(2), 986–988.

    Article  CAS  Google Scholar 

  • Du, T., Zhang, Y. A., Wang, Y. Z., Qu, L. J., Wang, Q. H., & Li, Z. L. (2014). Infectivity test on Esteya vermicola conidia against pine wood nematode. Forest Research, 27(2), 174–178.

    Google Scholar 

  • Fukuda, K. (1997). Physiological process of the symptom development and resistance mechanism in pine wilt disease. Journal of Forest Research, 2(3), 171–181.

    Article  Google Scholar 

  • Futai, K. (2008). Pine wilt in Japan: From first incidence to the present. In Pine wilt disease (pp. 5-12): Springer.

  • Kwiko Kuroda, A. K. (2016). Rish of killing uninfected pine trees by the repeated trunk-injection of nematicides to prevent pine wilt, 2016 IUFRO Working Party 7.02.10 Pine Wilt Disease International Symposium. Seoul, Korea.

  • Lin, F., Ye, J., Wang, H., Zhang, A., & Zhao, B. (2013). Host deception: Predaceous fungus, Esteya vermicola, entices pine wood nematode by mimicking the scent of pine tree for nutrient. PLoS One, 8(8), e71676.

    Article  CAS  Google Scholar 

  • Liou, J. Y., Shih, J. Y., & Tzean, S. S. (1999). Esteya, a new nematophagous genus from Taiwan, attacking the pinewood nematode (Bursaphelenchus xylophilus). Mycological Research, 103(2), 242–248.

    Article  Google Scholar 

  • Ma, T., Shi, X. H., Shen, J., et al. (2018). Field evaluation of commercial attractants and trap placement for monitoring pine sawyer beetle, Monochamus alternatus (Coleoptera: Cerambycidae) in Guangdong, China. Journal of Economic Entomology, 111(1), 239–246.

    Article  CAS  Google Scholar 

  • Shin, S. C., & Han, H. R. (2006). Current status on research and management of pine wilt disease in Korea. Paper presented at the proceedings of the international symposium on current status on research and management of pine wilt disease. Korea: Seoul.

    Google Scholar 

  • Togashi, K., & Matsunaga, K. (2004). A simple method for discriminating Bursaphelenchus xylophilus and B. mucronatus by species-specific polymerase chain reaction primer pairs. Nematology, 6(2), 273–277.

    Article  Google Scholar 

  • VanWoerkom, A. H., Aćimović, S. G., Sundin, G. W., Cregg, B. M., Mota-Sanchez, D., Vandervoort, C., et al. (2014). Trunk injection: An alternative technique for pesticide delivery in apples. Crop Protection, 65, 173–185.

    Article  CAS  Google Scholar 

  • Vicente, C., Espada, M., Vieira, P., & Mota, M. (2012). Pine wilt disease: A threat to European forestry. European Journal of Plant Pathology, 133(1), 89–99.

    Article  CAS  Google Scholar 

  • Wang, C. Y., Fang, Z. M., Sun, B. S., Gu, L. J., Zhang, K. Q., & Sung, C. (2008). High infectivity of an endoparasitic fungus strain, Esteya vermicola, against nematodes. The Journal of Microbiology, 46(4), 380–389.

    Article  Google Scholar 

  • Wang, C. Y., Fang, Z. M., Wang, Z., Gu, L. J., Sun, B. S., Zhang, D. L., et al. (2009a). High infection activities of two Esteya vermicola isolates against pinewood nematode. African Journal of Microbiology Research, 3(10), 581–584.

    Google Scholar 

  • Wang, C. Y., Wang, Z., La Lee, M., Li, Z., Zhang, D. L., Liu, L., et al. (2009b). Attraction of pinewood nematode, Bursaphelenchus xylophilus, to the endoparasitic fungus Esteya vermicola. African Journal of Microbiology Research, 3(11), 782–786.

    Google Scholar 

  • Wang, C. Y., Wang, Z., Fang, Z. M., Zhang, D. L., Gu, L. J., Liu, L., & Sung, C. K. (2010). Attraction of pinewood nematode to Endoparasitic Nematophagous fungus Esteya vermicola. Current Microbiology, 60(5), 387–392.

    Article  CAS  Google Scholar 

  • Wang, C. Y., Fang, Z. M., Wang, Z., Zhang, D. L., Gu, L. J., Lee, M. R., et al. (2011a). Biological control of the pinewood nematode Bursaphelenchus xylophilus by application of the endoparasitic fungus Esteya vermicola. BioControl, 56(1), 91–100.

    Article  Google Scholar 

  • Wang, Z., Wang, C. Y., Yang, Z. H., Fang, Z. M., Moon, Y. J., Sun, B. S., & Sung, C. (2011b). Viability and pathogenicity of Esteya vermicola in pine trees. Biocontrol Science and Technology, 21(4), 387–393.

    Article  Google Scholar 

  • Wang, Y., Yang, Z., Yu, J., Zhang, Y., Xue, J., Li, Z., Li, J. J., Wang, C. Y., Wang, Z., Hou, J. G., Begum, S., Gu, L. J., Lee, M. R., & Sung, C. K. (2013). Comparison between conidia and blastospores of Esteya vermicola, an endoparasitic fungus of the pinewood nematode, Bursaphelenchus xylophilus. World Journal of Microbiology and Biotechnology, 29(12), 2429–2436.

    Article  Google Scholar 

  • Wang, R., Dong, L., Chen, Y., Qu, L., Wang, Q., & Zhang, Y. (2017a). Esteya Vermicola, a Nematophagous fungus attacking the pine wood nematode, harbors a bacterial Endosymbiont affiliated with Gammaproteobacteria. Microbes and Environments, 32(3), 201–209.

    Article  Google Scholar 

  • Wang, Z., Zhang, Y., Wang, C., Wang, Y., & Sung, C. (2017b). Esteya vermicola controls the pinewood nematode, Bursaphelenchus xylophilus, in pine seedlings. Journal of Nematology, 49(1), 86–91.

    Article  CAS  Google Scholar 

  • Wang, C. Y., Yin, C., Fang, Z. M., Wang, Z., Wang, Y. B., Xue, J. J., et al. (2018). Using the nematophagous fungus Esteya vermicola to control the disastrous pine wilt disease. Biocontrol Science and Technology, 28(3), 268–277.

    Article  Google Scholar 

  • Xue, J., Hou, J., Zhang, Y., Wang, Y., Lee, M., Yu, J., & Sung, C. K. (2014). Optimization of promoting conidial production of a pinewood nematode biocontrol fungus, Esteya vermicola using response surface methodology. Current Microbiology, 69(5), 745–750.

    Article  CAS  Google Scholar 

  • Yin, C., Wang, Y., Zhang, Y., Wang, H., Tao, R., Li, Y., & Sung, C. K. (2019). A pine wood sample preparation method for high target and quality DNA extraction for detection of Esteya vermicola by PCR from living pine. Journal of Basic Microbiology, 59(4), 437–441.

    Article  CAS  Google Scholar 

  • Zhao, B. G. (2008). Pine wilt disease in China. In Pine wilt disease (pp. 18-25): Springer.

  • Zhao, B. G., Futai, K., Sutherland, J. R., & Takeuchi, Y. (2008). Pine wilt disease: Springer.

Download references

Acknowledgements

This research was funded by the National Natural Science Foundation of China (NSFC) under grant 31300545, and the Ministry of Science and Technology of the People’s Republic of China under grant 2017YFD0600102.

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, College of Agriculture and Biotechnology, Chungnam National University, Daejeon, 305-764, South Korea

    Can Yin, Yunbo Wang, Haihua Wang, Beibei Duan, Ran Tao, Jie Gao & Chang-keun Sung

  2. Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

    Yong-an Zhang

Authors
  1. Can Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yunbo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong-an Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haihua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Beibei Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ran Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jie Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chang-keun Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chang-keun Sung.

Ethics declarations

The authors declare no conflict of interest. This article does not contain any work conducted on animal or human participants. Informed consent was not applicable to this article since no information regarding individual participants was included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yin, C., Wang, Y., Zhang, Ya. et al. Hypothesized mechanism of biocontrol against pine wilt disease by the nematophagous fungus Esteya vermicola. Eur J Plant Pathol 156, 811–818 (2020). https://doi.org/10.1007/s10658-019-01930-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01930-9

Keywords

Search

Navigation