Tolerance to oxidative stress of inbred strains of the pine wood nematode, Bursaphelenchus xylophilus, differing in terms of virulence

in Nematology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Summary

The virulence of Bursaphelenchus xylophilus, the pine wood nematode, varies greatly among different populations. Two inbred strains, called P3 and P9, were recently established via repeated full-sib mating. They exhibited remarkable differences in pathogenicity-related traits. Although their propagation did not differ when cultured on fungal lawns, P9 reproduced better in host seedlings and exhibited higher virulence. In the present study, we obtained fundamental information about P3 and P9 in terms of tolerance to oxidative stress and examined this tolerance and the cuticular ultrastructure. P9 survived better under hydrogen peroxide (H2O2)-stressed conditions than did P3. In addition, P9 had a thicker cuticle than P3. Although further studies are needed, these results suggest that the difference in tolerance in P3 and P9 was due not only to physiological features, such as H2O2-degrading ability, but also to physical factors (cuticle thickness).

Nematology

International Journal of Fundamental and Applied Nematological Research

Sections

References

Abelleira, A., Picoaga, A., Mansilla, J.P. & Aguin, O. (2011). Detection of Bursaphelenchus xylophilus, causal agent of pine wilt disease on Pinus pinaster in northwestern Spain. Plant Disease 95, 766. DOI: 10.1094/PDIS-12-10-0902

Aebi, H. (1984). Catalase in vitro. Methods in Enzymology 105, 121-126. DOI: 10.1016/S0076-6879(84)05016-3

Aikawa, T. & Kikuchi, T. (2007). Estimation of virulence of Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) based on its reproductive ability. Nematology 9, 371-377. DOI: 10.1163/156854107781352007

Bird, A.F. & Bird, J. (1991). The structure of nematodes. California, USA, Academic Press.

Bird, A.F. & Buttrose, M.S. (1974). Ultrastructural changes in the nematode Anguina tritici associated with anhydrobiosis. Journal of Ultrastructure Research 48, 177-189. DOI: 10.1016/S0022-5320(74)80075-4

Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantitation of protein utilizing the principle of protein-binding. Analytical Biochemistry 72, 248-254. DOI: 10.1016/0003-2697(76)90527-3

Cheng, H.R., Lin, M., Li, W. & Fang, Z. (1983). The occurrence of a pine wilting disease caused by a nematode found in Nanjing. Forest Pest and Disease 4, 1-5.

Dwinell, L.D. & Nickle, W.R. (1989). An overview of the pine wood nematode ban in North America. United States Department of Agriculture Forest Service General Technical Report. SE 55. Asheville, NC, USA, Southeastern Forest Experiment Station. DOI: 10.2737/SE-GTR-55

Ekino, T., Yoshiga, T., Takeuchi-Kaneko, Y. & Kanzaki, N. (2017). Transmission electron microscopic observation of body cuticle structures of phoretic and parasitic stages of Parasitaphelenchinae nematodes. PLoS ONE 12, e179465. DOI: 10.1371/journal.pone.0179465

Futai, K. (2013). Pine wood nematode, Bursaphelenchus xylophilus. Annual Review of Phytopathology 51, 61-83. DOI: 10.1146/annurev-phyto-081211-172910

Kadoya, Y. (2010). [The practical method for ultrathin sectioning.] Tokyo, Japan, Nishimura Company Limited.

Kawaguchi, E. (2006). Relationship between the anatomical characteristics of cortical resin canals and migration of Bursaphelenchus xylophilus in stem cuttings of Pinus thunbergii seedlings. Journal of the Japanese Forest Society 88, 240-244. [In Japanese with an English abstract.] DOI: 10.4005/jjfs.88.240

Kiyohara, T., Dozono, Y., Hasimoto, H. & Ono, K. (1973). [Relationship between inoculum density and pathogenicity of pine wood nematode, Bursaphelenchus xylophilus.] Transactions of Kyushu Branch of the Japanese Forestry Society 26, 191-192.

Kojima, K., Kamijyo, A., Masumori, M. & Sasaki, S. (1994). [Cellulase activities of pine-wood nematode isolates with different virulence.] Journal of the Japanese Forest Society 76, 258-262.

Kondo, E. & Ishibashi, N. (1978). Ultrastructural differences between the propagative and dispersal forms in pine wood nematode, Bursaphelenchus lignicolus, with reference to the survival. Applied Entomology and Zoology 13, 1-11. DOI: 10.1303/aez.13.1

Li, Z., Liu, X., Chu, Y., Wang, Y., Zhang, Q. & Zhou, X. (2011). Cloning and characterization of a 2-cys peroxiredoxin in the pine wood nematode, Bursaphelenchus xylophilus, a putative genetic factor facilitating the infestation. International Journal of Biological Sciences 7, 823-836. DOI: 10.7150/ijbs.7.823

Linit, M.J. (1990). Transmission of pinewood nematode through feeding wounds of Monochamus carolinensis (Coleoptera: Cerambycidae). Journal of Nematology 22, 231-236.

Mamiya, Y. (1975). The life history of the pine wood nematode, Bursaphelenchus lignicolus. Japanese Journal of Nematology 5, 16-25.

Mamiya, Y. (1988). History of pine wilt disease in Japan. Journal of Nematology 20, 219-226.

Mamiya, Y. (1990). Behavior of the pine wood nematode, Bursaphelenchus xylophilus, and disease development in pine trees. Nippon Nogeikagaku Kaishi 64, 1243-1246. DOI: 10.1271/nogeikagaku1924.64.1243

Morimoto, K. & Iwasaki, A. (1972). [Role of Monochamus alternatus (Coleoptera: Cerambycidae) as a vector of Bursaphelenchus lignicolus.] Journal of the Japanese Forest Society 54, 177-183. DOI: 10.11519/jjfs1953.54.6_177

Mota, M.M., Braasch, H., Bravo, M.A., Penas, A.C., Burgermeister, W., Metge, K. & Sousa, E. (1999). First report of Bursaphelenchus xylophilus in Portugal and in Europe. Nematology 1, 727-734. DOI: 10.1163/156854199508757

Palomares-Rius, J.E., Tsai, I.J., Karim, N., Akiba, M., Kato, T., Maruyama, H., Takeuchi, Y. & Kikuchi, T. (2015). Genome-wide variation in the pinewood nematode Bursaphelenchus xylophilus and its relationship with pathogenic traits. BMC Genomics 16, 845. DOI: 10.1186/s12864-015-2085-0

Rasband, W.S. (2014). ImageJ, US. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/.

Sato, H., Sakuyama, T. & Kobayashi, M. (1987). [Transmission of Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle (Nematoda, Aphelenchoididae) by Monochamus saltuaris (Gebler) (Coleoptera, Cerambycidae).] Journal of the Japanese Forest Society 69, 492-496.

Shinya, R., Takeuchi, Y. & Futai, K. (2009). A technique for separating the developmental stages of the propagative form of the pine wood nematode, Bursaphelenchus xylophilus. Nematology 11, 305-307. DOI: 10.1163/156854108X399164

Shinya, R., Morisaka, H., Takeuchi, Y., Ueda, M. & Futai, K. (2010). Comparison of the surface coat proteins of pine wood nematode appeared during host pine infection and in vitro culture by a protein approach. Phytopathology 100, 1289-1297. DOI: 10.1094/PHYTO-04-10-0109

Shinya, R., Takeuchi, Y., Ichimura, K., Takemoto, S. & Futai, K. (2012). Establishment of a set of inbred strains of the pine wood nematode, Bursaphelenchus xylophilus (Aphelenchida: Aphelenchoididae), and evidence of their varying levels of virulence. Applied Entomology and Zoology 47, 341-350. DOI: 10.1007/s13355-012-0124-8

Shinya, R., Morisaka, H., Kikuchi, T., Takeuchi, Y., Ueda, M. & Futai, K. (2013). Secretome analysis of the pine wood nematode Bursaphelenchus xylophilus reveals the tangled roots of parasitism and its potential for molecular mimicry. PLoS ONE 8, e67377. DOI: 10.1371/journal.pone.0067377

Vicente, C.S.L., Ikuyo, Y., Mota, M. & Hasegawa, K. (2013). Pinewood nematode-associated bacteria contribute to oxidative stress resistance of Bursaphelenchus xylophilus. BMC Microbiology 13, 299. DOI: 10.1186/1471-2180-13-299

Vicente, C.S.L., Ikuyo, Y., Shinya, R., Mota, M. & Hasegawa, K. (2015). Catalase induction in high virulence pinewood nematode Bursaphelenchus xylophilus under hydrogen peroxide-induced stress. PLoS ONE 10, e0123839. DOI: 10.1371/journal.pone.0123839

Wharton, D.A. (1996). Water loss and morphological changes during desiccation of the anhydrobiotic nematode Ditylenchus dipsaci. Journal of Experimental Biology 199, 1085-1093.

Yi, C.K., Byun, B.H., Park, J.D., Yang, S.I. & Chang, K.H. (1989). First finding of the pine wood nematode, Bursaphelenchus xylophilus (Steiner et Buhrer) Nickle and its insect vector in Korea. Research Reports of the Forestry Research Institute 38, 141-149. [Abstr.]

Yu, L., Wu, X., Ye, J., Zhang, S. & Wang, C. (2012). NOS-like-mediated nitric oxide is involved in Pinus thunbergii response to the invasion of Bursaphelenchus xylophilus. Plant Cell Reports 31, 1813-1821. DOI: 10.1007/s00299-012-1294-0

Figures

  • Survival of Bursaphelenchus xylophilus P3 (an avirulent strain) and P9 (a virulent strain) immersed in hydrogen peroxide (H2O2) solutions. A: Second-stage propagative juveniles; B: Third-stage propagative juveniles; C: Fourth-stage propagative juveniles; D: Adults. The means of 15 replications (with standard deviations) are shown. Asterisks indicate significant differences between P3 and P9 (Student’s t-test, *P<0.05, **P<0.01).

    View in gallery
  • Survival of Bursaphelenchus xylophilus P3 (an avirulent strain; grey lines) and P9 (a virulent strain; black lines) immersed in 40 mM H2O2. The means derived from 15 replications (with standard deviations) are shown. The letters a, b, c and x, y, z indicate significant differences between stages (Student’s t-test; P<0.001). Stages are: second- (J2), third- (J3) and fourth-stage (J4) propagative juveniles.

    View in gallery
  • Catalase activities of the Bursaphelenchus xylophilus P3 avirulent strain and the P9 virulent strain immersed in H2O2 solutions. The data are from five replications (with standard errors) are shown. n.s. = not significant (Student’s t-test; P>0.05).

    View in gallery
  • Electron micrographs of Bursaphelenchus xylophilus males (EPI = epicuticle; CZ = cortical + median zone; BZ = basal zone). A: P3 (an avirulent strain); B: P9 (a virulent strain). (Scale bars = 200 nm.)

    View in gallery
  • Cuticular zone measurements of adults of Bursaphelenchus xylophilus P3 (an avirulent strain) and P9 (a virulent strain).

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 12 12 12
Full Text Views 4 4 4
PDF Downloads 2 2 2
EPUB Downloads 0 0 0