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Adaptation of pine wood nematode, Bursaphelenchus xylophilus, early in its interaction with two Pinus species that differ in resistance

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Abstract

Pine wilt disease (PWD) is one of the most devastating diseases of Pinus spp. and is caused by the pine wood nematode (PWN), Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle. To study adaptation of PWN to survive in hosts that differ in resistance, we examined the self-regulatory characteristics of PWN at the biological and molecular levels early in the interaction. Two-year-old susceptible Pinus thunbergii and resistant Pinus taeda were selected for this experiment, and changes in PWNs after inoculation were assessed. qRT-PCR was used to detect changes in genes related to PWN pathogenicity and detoxification. The results showed that the migration and reproductive abilities of PWNs in P. thunbergii were stronger than those of PWNs in P. taeda. After 7 d, the number of nematodes in P. thunbergii was approximately 3.2-fold higher than in P. taeda. After 15 d, the number of nematodes in P. thunbergii was approximately twofold higher than that in P. taeda. Because PWN can adjust its sex ratio after infection, we compared the sex ratio of uninoculated PWNs, to that in the two pine species. In P. thunbergii, the female to male ratio first decreased and then stabilized over time; in P. taeda first decreased and then increased. Relative fat accumulation in PWNs increased significantly after the PWNs entered the tree body; the accumulation rate in P. thunbergii was higher than in P. taeda at 7 d, but lower after 15 d. Scanning electron microscopy (SEM) showed significantly more bacteria on the surface of PWNs in P. taeda compared with PWNs in susceptible P. thunbergii. At 12 h after inoculation, the expression of genes related to cell-wall degradation (BxBeta1-4 and Bxpel1), effectors (BxCDP1, BxSapB1), and active oxygen metabolism (Bxy-ctl-1 and BxGST3) was 2–6 × higher in the resistant pine than in the susceptible one. In contrast, in PWNs, the expression of autophagy-related genes BxATG1 and BxATG16 was 1.5–2 times higher in P. thunbergii than in P. taeda. These results indicate that the interaction between PWNs and pine trees with different resistance levels elicits a series of physiological and molecular adaptations that affect nematode reproduction and virulence. This study will help elucidate the adaptive mechanisms of PWN in different pine trees.

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References

  • Boya P, Reggiori F, Codogno P (2013) Emerging regulation and functions of autophagy. Nat Cell Biol 15(8):713–720

    Article  CAS  Google Scholar 

  • Deng LN, Wu XQ (2016) Research on the relationship of autophagy with the virulence and development of Bursaphelenchus xylophilus. J Nanjing for Univ (nat Sci Edn) 40(04):171–176

    CAS  Google Scholar 

  • Fu HY, Ren JH, Huang L, Li H, Ye JR (2014) Screening and functional analysis of the peroxiredoxin specifically expressed in Bursaphelenchus xylophilus The causative agent of pine wilt disease. Int J Mol Sci 15(6):10215–10232

    Article  CAS  Google Scholar 

  • Fu YM, Liu HB, Wu XQ (2020) Diversity and function of endo-bacteria in Bursaphelenchus xylophilus from Pinus massoniana Lamb in different regions. Forests 11(5):487

    Article  Google Scholar 

  • Fukuda K (1997) Physiological Process of the symptom development and resistance mechanism in pine wilt disease. J Forest Res (jpn) 2(3):171–181. https://doi.org/10.1007/BF02348216

    Article  Google Scholar 

  • Gabriel P, Neves PD, Romeu F, Paula V, Santos SS, Luís F, Abrantes I, Morais PV, Daniel G (2013) Nematicidal bacteria associated to pinewood nematode produce extracellular proteases. PloS One 8(11):e79705

    Article  Google Scholar 

  • He LX, Wu XQ, Yu LZ, Ji J, Ye JR (2010) The difference of H2O2 and oxidative enzyme in the interaction of different resistance pines and Bursaphelenchus xylophilus. J Nanjing Univ (nat Sci Edn) 34(6):13–17. https://doi.org/10.3969/j.issn.1000-2006.2010.06.004(inChinese)

    Article  CAS  Google Scholar 

  • He LX, Xue Q, Wu XQ (2016) Effects of endobacteria on reproduction and virulence of Bursaphelenchus xylophilus. J Nanjing For Univ (Nat Sci Edn). https://doi.org/10.3969/j.issn.1000-2006.2016.03.008

    Article  Google Scholar 

  • Hu LJ, Wu XQ, Li HY, Zhao QY, Wang YC, Ye JR (2019) An effector BxSapB1 induces cell death and contributes to virulence in the pine wood nematode Bursaphelenchus xylophilus. Mol Plant Microbe Interact 32(4):452–463

    Article  CAS  Google Scholar 

  • Hu LJ, Wu XQ, Li HY, Wang YC, Huang X, Wang Y, Li Y (2020) BxCDP1 from the pine wood nematode Bursaphelenchus xylophilus is recognized as a novel molecular pattern. Mol Plant Pathol 21(7):923–935

    Article  CAS  Google Scholar 

  • Huang XW, Liu JW, Ding JM, He QS, Xiong R, Zhang KQ (2009) The investigation of nematocidal activity in Stenotrophomonas maltophilia G2 and characterization of a novel virulence serine protease. Can J Microbiol 55:934–942. https://doi.org/10.1139/W09-045

    Article  CAS  PubMed  Google Scholar 

  • Ichihara Y, Fukuda K, Suzuki K (1999) Migration of pine wood nematode, Bursaphelenchus xylophilus, in Japanese black pine seedlings, Pinus thunbergii, in relation to early symptom of pine wilt disease. Sustainability of Pine Forests in Relation to Pine Wilt & Decline International Symposium.

  • Jin G (2007) Ye JR (2007) Histopathological study on the nematode in Seedling of Pinus thunbergii. J Nanjing for Univ (nat Sci Edn) 031(004):115–120 ((in Chinese))

    Google Scholar 

  • Jones JT, Moens M, Mota M, Hongmei LI, Kikuchi T (2010) Bursaphelenchus xylophilus: opportunities in comparative genomics and molecular host-parasite interactions. Mol Plant Pathol 9(3):357–368

    Article  Google Scholar 

  • Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Berriman M (2011) Genomic insights into the origin of parasitism in the emerging plant pathogen. Plos Pathog 7(9):e1002219

    Article  CAS  Google Scholar 

  • Kobayashi T, Sasaki K, Mamiya Y (1974) Fungi associated with Bursaphelenchus lignicolus, the pine wood nematode. J Jpn For Soc 56:136–145

    Google Scholar 

  • Li YX, Zhang XY (2018) Research advance of pathogenic mechanism of pine wilt disease. Huan Jing Kun Chong Xue Bao 40(02):231–241 (in Chinese)

    CAS  Google Scholar 

  • Li Z, Liu XX, Chu YN, Wang Y, Zhang QW, Zhou XG (2011) Cloning and characterization of a 2-Cys peroxiredoxin in the pine wood nematode, Bursaphelenchus xylophilus, a putative genetic factor facilitating the infestation. Int J Biol Sci 7(6):823–836

    Article  CAS  Google Scholar 

  • Li YX, Wang Y, Liu ZY, Wang X, Lu Q, Jia XZ, Zhang XY (2016) Functional analysis of the venom allergen-Like protein gene from pine wood nematode Bursaphelenchus xylophilus using a baculovirus expression system. Physiol Mol Plant Pathol 93:58–66

    Article  CAS  Google Scholar 

  • Liu HB, Rui L, Feng YQ, Wu XQ (2019a) Molecular Characterization and functional analysis of three autophagy genes, BxATG5, BxATG9, and BxATG16 Bursaphelenchus Xylophilus. Int J Mol Sci 20(15):3769. https://doi.org/10.3390/ijms20153769

    Article  CAS  PubMed Central  Google Scholar 

  • Liu HB, Wu F, Wu XQ, Ye JR (2019b) Differential effects of rapamycin on Bursaphelenchus xylophilus with different virulence and differential expression of autophagy genes under stresses in nematodes. Acta Biochim Biophys Sin 3:254–262. https://doi.org/10.1093/abbs/gmy172(inChinese)

    Article  Google Scholar 

  • Liu HB, Rui L, Feng YQ, Wu XQ (2020) Autophagy contributes to resistance to the oxidative stress induced by pine reactive oxygen species metabolism, promoting infection by Bursaphelenchus xylophilus. Pest Manag Sci 76(8):2755–2767. https://doi.org/10.1002/ps.5823

    Article  CAS  PubMed  Google Scholar 

  • Livak K, Schmittgen D (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Ma HB (2008) Study on the cloning and RNA interference of the cellulase system of pine wood nematode Bursaphelenchus xylophilus and its cDNA gene. Dissertation, Chinese Academy of Forestry. (in Chinese)

  • Ma HB, Lu Q, Liang J, Zhang XY (2011) Functional analysis of the cellulose gene of the pine wood nematode, Bursaphelenchus xylophilus, using RNA interference. Genet Mol Res 10(3):1931–1941. https://doi.org/10.4238/vol10-3gmr1367

    Article  CAS  PubMed  Google Scholar 

  • Margarida E, Sebastian EVDA, Tom M, Vijayapalani P, Thomas B, Manuel M, Jones JT (2018) STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus Xylophilus. BMC Genomics 19(1):553. https://doi.org/10.1186/s12864-018-4908-2

    Article  CAS  Google Scholar 

  • Mizushima N (2005) The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ 12(2):1535–1541. https://doi.org/10.1038/sj.cdd.440172

    Article  CAS  PubMed  Google Scholar 

  • Mota MM, Vieira PR (2009) Pine wilt disease: a world-wide threat to forest ecosystems. Nematology 11(2):315–316

    Article  Google Scholar 

  • Nascimento FX, Hasegawa K, Mota M, Vicente CS (2015) Bacterial role in pine wilt disease development-Review and future perspectives. Environ Microbiol 7(1):51–63. https://doi.org/10.1111/1758-2229.12202

    Article  Google Scholar 

  • Nian B (2017) Cloning and functional analysis of glutathione S-transferase gene BxGST3 and BxGST1 in Bursaphelenchus xylophilus. Dissertation, Nanjing Forestry University. (in Chinese)

  • Proença DN, Grass G, Morais PV (2017) Understanding pine wilt disease: Roles of the pine endophytic bacteria and of the bacteria carried by the disease-causing pinewood nematode. Microbiology Open 6(2):e00415. https://doi.org/10.1002/mbo3.415

    Article  Google Scholar 

  • Rui L, Liu HB, Liang R, Wu XQ (2021) Resistance genes mediate differential resistance to pine defensive substances α-Pinene and H2O2 in Bursaphelenchus xylophilus with different levels of virulence. J for Res 32:1753–1762. https://doi.org/10.1007/s11676-020-01182-y

    Article  CAS  Google Scholar 

  • Santos CS, Pinheiro M, Silva AI, Egas C, Vasconcelos MW (2012) Searching for resistance genes to Bursaphelenchus xylophilus using high throughput screening. BMC Genomics 13(1):599. https://doi.org/10.1186/1471-2164-13-599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smant G, Stokkermans J, Yan Y, Boer DJM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL (1998) Endogenous cellulases in animals: isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. P Natl A Sci India B 95:4906–4911. https://doi.org/10.1016/1369-5266(88)80030-X

    Article  CAS  Google Scholar 

  • Son JA, Komatsu M, Matsushita N, Hogetsu T (2010) Migration of pine wood nematodes in the tissues of Pinus thunbergii. J Forest Res (jpn) 15(3):186–193. https://doi.org/10.1007/s10310-009-0171-3

    Article  CAS  Google Scholar 

  • Vicente CSL, Ikuyo Y, Shinya R, Mota M, Hasegawa K (2014) Virulence and oxidative stress response of the pine wood nematode Bursaphelenchus Xylophilus. J Nematol 46:252–252

    Google Scholar 

  • Vicente CSL, Yoriko I, Ryoji S, Mota M, Hasegawa K (2015) Catalases induction in high virulence pinewood nematode Bursaphelenchus xylophilus under hydrogen peroxide-induced stress. PLoS ONE 10(4):e0123839. https://doi.org/10.1371/journal.pone.0123839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viglierchio DR, Schmitt RV (1983) On the methodology of nematode extraction from field samples: Baermann funnel modifications. J Nematol 15:438–444

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SL, Cao FX, Wang M, Qian WQ (2009) Research advance of Bursaphelenchus xylophilus genes. Journal of Central South University of Forestry & Technology 29(3)

  • Wang BW, Liu WL, Wang F, Ma L, Li DL, Wang BY, Hao X (2017) Fat accumulation in Bursaphelenchus xylophilus by positively regulating Bx-SCD under low temperature. J Nanjing For Univ 45(7):89–93

    Google Scholar 

  • Wei Y, Liu Q, Zhou Z, Xu LY, Chen XL, Hao YP (2018) Changes of chemical signals in needles of Pinus massoniana with different resistance after inoculation of pine wood nematode. Scientia Silvae Sinicae 54(2):119–125

    CAS  Google Scholar 

  • Wu DQ (2015) Cloning of the new effector Ha-G20E03 gene of cereal cyst nematode and exploration of a new model system for the function. Dissertation, Chinese Academy of Sciences

  • Wu F, Wu XQ (2018) The role of autophagy of pine wood nematode Bursaphelenchus xylophilus in the growth and development and infecting pine trees at early time. J Nanjing for Univ (nat Sci Edn) 61(05):59–64. https://doi.org/10.3969/j.issn.1000-2006.201712025(inChinese)

    Article  Google Scholar 

  • Wu XQ, Yuan WM, Tian XJ, Fan B, Fang X, Ye JR, Ding XL (2013) Specific and functional diversity of endophytic bacteria from pine wood nematode Bursaphelenchus Xylophilus with different virulence. Int J Biol Sci 9(1):34–44. https://doi.org/10.7150/ijbs.5071

    Article  CAS  PubMed  Google Scholar 

  • Xie WF, Li HM, Huang AZ, Feng LZ (2017) The dynamic change of gene expression from Pinus massoniana in response to Bursaphelenchus xylophilus infestation. Fujian J Agri Sci. https://doi.org/10.19303/j.issn.1008-0384.2017.04.010

    Article  Google Scholar 

  • Xue Q, Xiang Y, Wu XQ, Li MJ (2019) Bacterial communities and virulence associated with pine wood nematode Bursaphelenchus xylophilus from different Pinus spp. Int J Mol Sci 20(13):3342. https://doi.org/10.3390/ijms20133342

    Article  CAS  PubMed Central  Google Scholar 

  • Yang BJ (1995) The prevalence and control of pine wood nematode disease in China. China Forestry Publishing House, Beijing (in Chinese)

    Google Scholar 

  • Yang BJ, Pan HY, Tang J, Wang YY, Wang LF (2003) Pine wood nematode disease. Beijing: China Forestry Publishing House, pp. 45–48.

  • Ye JR (2019) Epidemic status of pine wilt disease in China and its prevention and control techniques and counter measures. Scientia Silvae Sinicae 55(9):1–10 (in Chinese)

    Google Scholar 

  • Yin YN, Wu JW, Tan JJ, Hao DJ (2020) Optimization of medium and culture conditions for Bacillus cereus NJSZ-13. J Zhejiang Forest Sci Technol 40(6):12–20 (in Chinese)

    Google Scholar 

  • Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53(8):1355–1365. https://doi.org/10.1093/pcp/pcs099

    Article  CAS  PubMed  Google Scholar 

  • Zas R, Moreira X, Ramos M, Lima MRM, Silva MND, Solla A, Vasconcelos MW, Sampedro L (2015) Intraspecific variation of anatomical and chemical defensive traits in Maritime pine (Pinus pinaster) as factors in susceptibility to the pine wood nematode (Bursaphelenchus xylophilus). Trees-Struct Funct 29(3):663–673. https://doi.org/10.1007/s00468-014-1143-6

    Article  Google Scholar 

  • Zhang H, Wu F, Wang XW, Du HW, Wang XC, Zhang H (2013) The two C elegans ATG-16 homologs have partially redundant functions in the basal autophagy pathway. Autophagy 9(12):1965–1974

    Article  CAS  Google Scholar 

  • Zhao LJ (2015) Epigenetic study on glucose-induced fat deposition in nematodes. Dissertation, Hefei University of Technology. https://doi.org/10.7666/d.Y2925607

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Correspondence to Xiaoqin Wu.

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Project Funding: The work was supported by the major emergency project in science and technology of National Forestry and Grassland Administration (ZD202001) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Corresponding Editor: Tao Xu.

The original online version of this article was revised: “There are several errors in the supplementary material that were caused during production process". The correct files and links are given below.

The original online version of this article was revised: The corresponding author was incorrectly identified as Xinyu Wang during the production process. The corresponding author should be Xiaoqin Wu.

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Feng, Y., Rui, L., Wang, X. et al. Adaptation of pine wood nematode, Bursaphelenchus xylophilus, early in its interaction with two Pinus species that differ in resistance. J. For. Res. 33, 1391–1400 (2022). https://doi.org/10.1007/s11676-021-01416-7

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