Abstract
Bursaphelenchus xylophilus is the pathogen that causes pine wilt disease, which has greatly damaged forests and ecosystems in countries of East Asia and Europe. Bursaphelenchus mucronatus is closely related to B. xylophilus in morphology and host plant specificity. A long-running debate has existed regarding whether these two species can successfully produce hybrid offspring. In the present study, we performed in the laboratory, hybridization of two B. xylophilus nematode isolates from China and Japan and three B. mucronatus isolates from China, Japan and France. Nematode isolates of B. xylophilus were successfully crossed with B. mucronatus isolates, and the rate of hybridization was relatively high; however, some hybrid offspring died. Successful hybridization occurred between B. xylophilus and B. mucronatus isolates from China, and 22 generations of hybrids were produced. All F1 hybrids could be backcrossed with their parents and produce offspring. Variation in mucro length among the hybrid offspring and their parents was observed. The hybrid offspring and their parents were inoculated into 3-months-old black pine (Pinus tunbergii) seedlings. Weaker pathogenicity of hybrid offspring was observed compared with that of their parents, and significantly fewer offspring nematodes than parents were reisolated from pines. Therefore, the offspring of B. xylophilus and B. mucronatus may exist in the forest and could influence disease epidemics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abad P, Tares S, Brugier N, Guiran GD (1991) Characterization of the relationships in the pinewood nematode species complex (PWNSC) (Bursaphelenchus spp.) using a heterologous unc-22 DNA probe from Caenorhabditis elegans. Parasitology 102(2):303–308
Ailing B, Guo Y, Han ZM (2010) Hybridization between Bursaphelenchus xylophilus and B. mucronatus and the pathogenicity of the offspring. Sci Silvae Sin 46(8):114–119
Baujard P (1980) Three new species of Bursaphelenchus (Nematoda: Tylenchida) and observations on the genus. Revue De Nematol 3(2):167–177
Bergdahl D (1988) Impact of pinewood nematode in North America: present and future. J Nematol 20(2):260–265
Bolla RI, Boschert M (1993) Pinewood nematode species complex: interbreeding potential and chromosome number. J Nematol 25(2):227–238
Braasch H (1994) Intra-and interspecific crossing experiments with a German and a Siberian isolate of Bursaphelenchus mucronatus (Nematoda: Aphelenchoididae) and related Bursaphelenchus species. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 46(12):276–281
Braasch H (2001) Bursaphelenchus species in conifers in Europe: distribution and morphological relationships. OEPP/EPPO Bull 31:127–142
Cheng HR, Lin MS, Qian RJ (1986) A study on the morphological diagnosis and the pathogenicity of Bursaphelenchus mucronatus. J Nanjing Agric Univ 9(2):55–61
Fang GM (1996) Bursaphelenchus mucronatus caused pine wilt. Jiangxi For Sci Technol 23(1):31–35
Fuchs AG (1937) Neue parasitische und halbparasitische Nematoden bei Borkenkäfern und einige andere Nematoden. Zoologische Jahrbücher, Abteilung für Systematik, Öekologie und Geographieder Tiere 70:291–380
Futai K (2013) Pine Wood Nematode, Bursaphelenchus xylophilus. Annu Rev Phytopathol 51:61–83
Goodey JB (1960) The classification of the Aphelenchoidea Fuchs 1937. Nematologica 5(2):111–126
Guiran GD, Bruguier N (1989) Hybridization and phylogeny of the pine wood nematode (Bursaphelenchus spp.). Nematologica 353:321–330
Hajdukiewicz PT, Myers RF (1988) Experimental crossing of selected isolates of Bursaphelenchus xylophilus and B. mucronatus. Phytopathology 78(11):1507–1508
Kanzaki N, Maehara N, Akiba M, Tanaka SE, Ide T (2016) Morphological characters of dauer juveniles of three species of Bursaphelenchus Fuchs, 1937. Nematology 18(2):209–220
Li GX, Li DL, Yu SF (2007) Preliminary investigation on the primary reason of pine wilt disease in Huaping. J Yunnan Agric Univ 22(2):225–228
Liao SM, Kasuga S, Togashi K (2014) Suppressive effects of Bursaphelenchus mucronatus on pine wilt disease development and mortality of B. xylophilus-inoculated pine seedlings. Nematology 16(2):219–227
Liu W, Yang BJ (1994) Hybridization between Bursaphelenchus xylophilus and B. mucronatus. For Res 7(5):469–473
Liu W, Yang BJ (1995) Comparison on the Shape of Male Spicules between Bursaphelenchus xylophilus and B. mucronatus. For Res 8(2):223–225
Ma CZ, Qian ZG, Gu ZR, Song JR, Chen PS (1996) Discovery of a “M”-Form isolate of nematode (Bursaphelenchus xylophilus) from dying pine trees (Pinus thunbergii) on Sheshan mountain in Shanghai. Acta Agric Shanghai 12(1):56–60
Mamiya Y (1986) Interspecific hybridization between Bursaphelenchus xylophilus and B. mucronatus (Aphelenchida: Aphelenchoididae). Appl Entomol Zool 21:159–163
Mamiya Y (1988) History of pine wilt disease in Japan. J Nematol 20(20):219–226
Mamiya Y, Enda N (1979) Bursaphelenchus mucronatus n.sp. (Nematoda: Aphelenchoididae) from pine wood and its biology and pathogenicity to pine trees. Nematologica 3(3):353–361
Nickle WR, Golden AM, Mamiya Y, Wergin WP (1981) On the Taxonomy and Morphology of the pine wood Nematode, Bursaphelenchus xylophilus (Steiner & Buhrer 1934) Nickle 1970. J Nematol 13(3):385–392
Queiroz KD (2005) Ernst Mayr and the modern concept of species. Proc Natl Acad Sci 102(Suppl 1):6600–6607
Riga E, Beckenbach K, Webster JM (1992) Taxonomic relationships of Bursaphelenchus xylophilus and B. mucronatus based on interspecific and intraspecific cross-hybridization and DNA analysis. Fundam Appl Nematol 15(5):391–395
Ryss A, Vieira P, Mota M, Kulinich O (2005) A synopsis of the genus Bursaphelenchus Fuchs, 1937 (Aphelenchida: Parasitaphelenchidae) with keys to species. Nematology 7(3):393–458
Ryss A, Polyanina KS, Popovichev BG, Krivets SA, Kerchev IA (2018) Plant host range specificity of Bursaphelenchus mucronatus mamiya et enda, 1979 tested in the laboratory experiments. Parazitologiia 52(1):32–40
Steiner G, Buhrer EM (1934) Aphelenchoides xylophilus n. sp., a nematode associated with blue-stain and other fungi in timber. J Agric Res 48(1):949–951
Wingfield MJ, Blanchette RA (1983) The pine-wood Nematode, Bursaphelenchusxylophilus, in Minnesota and Wisconsin: insect associates and transmission studies. Can J For Res 13(6):1068–1076
Yang BJ (2003) Pine Wilt Disease. Chinese Forestry Publishing House, Beijing, pp 1–4
Zhang ZY, Lin MS, Yu BY (2004) Pathogenicity of Bursaphelenchus mucronatus on the seedlings of black pine. J Nanjing Agric Univ 27(1):46–50
Zhang ZY, Chen X, Zhang YX, Liu AH, Chen CF (2008) A Study on the diversity of tail shape of Bursaphelenchus mucronatus. Plant Quar 22(2):73–75
Zhao LR, Liao JL, Zhong GQ (2005) A rapid method to detect Bursaphelenchus xylophilus and B. mucronatus by PCR. J South China Agric Univ 26(2):59–61
Acknowledgements
This work and its publication were supported by the special research program for non-profit forestry of the State Forestry Administration (201204501) by National Nature Science Foundation of China (31170600) and A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Author information
Authors and Affiliations
Corresponding author
Additional information
Project funding: This work were supported by the special research program for non-profit forestry of the State Forestry Administration (201204501), National Nature Science Foundation of China (31170600), and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
The online version is available at http://www.springerlink.com
Corresponding editor: Chai Ruihai.
Rights and permissions
About this article
Cite this article
Liu, KC., Ben, A., Han, Z. et al. Interspecific hybridization between Bursaphelenchus xylophilus and Bursaphelenchus mucronatus. J. For. Res. 30, 699–707 (2019). https://doi.org/10.1007/s11676-018-0658-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11676-018-0658-x