Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-26T07:07:09.573Z Has data issue: false hasContentIssue false
  • English
  • Français

Pine chemical volatiles promote dauer recovery of a pine parasitic nematode, Bursaphelenchus xylophilus

Published online by Cambridge University Press:  17 September 2019

Wei Zhang Open the ORCID record for Wei Zhang [Opens in a new window] ,
Yongxia Li ,
Long Pan ,
Xuan Wang ,
Yuqian Feng  and
Xingyao Zhang
Wei Zhang
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
Yongxia Li*
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
Long Pan
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
Xuan Wang
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
Yuqian Feng
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
Xingyao Zhang
Affiliation:
Lab. of Forest Pathogen Integrated Biology, Research Institute of Forestry New Technology, Chinese Academy of Forestry, Beijingl00091, China Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing210037, China
*
Author for correspondence: Yongxia Li, E-mail: liyongxiaxjs@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Pinewood nematode, Bursaphelenchus xylophilus, a pine parasitic nematode, poses a serious threat to its host pine forests globally. When dispersal-stage larvae 4 (dauer, DL4) of B. xylophilus enters the new pine, it moults into propagative adult (dauer recovery) and reproduces quickly to kill the host pine. Here, we found pine chemical volatiles, rather than the common dauer recovery factors of nematodes (e.g. suitable temperatures, nutrient availability or density), promote B. xylophilus dauer recovery. The results showed that volatilization of chemicals in host pines could attract DL4 and promote DL4 recovery. To identify which chemicals promote this process, we determined the stimulated activity of the main volatiles of pines including six monoterpenes and two sesquiterpenes. Results showed that all the six monoterpenes promoted dauer recovery, especially β-pinene and β-myrcene, but the two sesquiterpenes have no effect on the transformation. Furthermore, β-pinene performed gradient effects on dauer recovery. We hypothesized that when DL4 infect pine trees, the pine volatiles released from the feeding wounds are used as chemical signals for DL4 transformation to adult to reproduce and rapidly kill the pines. Our study identified the B. xylophilus dauer recovery chemical signal and may contribute to preventing pine wilt disease.

Keywords

Chemical volatilesdauer recoverypine wood nematodetransformation
Type
Research Article
Information
Parasitology , Volume 147 , Issue 1 , January 2020 , pp. 50 - 57
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aumann, J and Ehlers, R-U (2001) Physico-chemical properties and mode of action of a signal from the symbiotic bacterium Photorhabdus luminescens inducing dauer juvenile recovery in the entomopathogenic nematode Heterorhabditis bacteriophora. Nematology 3, 849–853.Google Scholar
Chen, R, He, X, Chen, J, Gu, T, Liu, P, Xu, T, Teale, SA and Hao, D (2018) Traumatic resin duct development, terpenoid formation, and related synthase gene expression in Pinus massoniana under feeding pressure of Monochamus alternatus. Journal of Plant Growth Regulation, 1–12.Google Scholar
Cheng, H, Lin, M, Li, W and Fang, Z (1983) The occurrence of a pine wilting disease caused by a nematode found in Nanjing. Forest Pest and Disease 4, 1–5.Google Scholar
Dolan, KM, Jones, JT and Burnell, AM (2003) Detection of changes occurring during recovery from the dauer stage in Heterorhabditis bacteriophora. Parasitology 125, 71–81.CrossRefGoogle Scholar
Fan, J, Sun, J and Shi, J (2007) Attraction of the Japanese pine sawyer, Monochamus alternatus, to volatiles from stressed host in China. Annals of Forest Science 64, 67–71.CrossRefGoogle Scholar
Fielenbach, N and Antebi, A (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes & Development 22, 2149–2165.CrossRefGoogle ScholarPubMed
Fukushige, H (1991) Propagation of Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) on Fungi Growing in Pine-Shoot Segments. Applied Entomology and Zoology 26, 371–376.CrossRefGoogle Scholar
Futai, K (2013) Pine wood nematode, Bursaphelenchus xylophilus. Annual Review of Phytopathology 51, 61–83.CrossRefGoogle ScholarPubMed
Golden, J and Riddle, D (1982) A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218, 578–580.CrossRefGoogle ScholarPubMed
Golden, JW and Riddle, DL (1984) The Caenorhabditis elegans dauer larva – developmental effects of pheromone, food, and temperature. Developmental Biology 102, 368–378.CrossRefGoogle ScholarPubMed
Hansen, SC, Stolter, C, Imholt, C and Jacob, J (2017) Like or dislike: response of rodents to the odor of plant secondary metabolites. Integrative Zoology 12, 428–436.CrossRefGoogle ScholarPubMed
Hinode, Y, Shuto, Y and Watanabe, H (1987) Stimulating effects of β-myrcene on molting and multiplication of the pine wood nematode, Bursaphelenchus xylophilus. Agricultural and Biological Chemistry 51, 1393–1396.Google Scholar
Hirao, A and Ehlers, RU (2010) Influence of inoculum density on population dynamics and dauer juvenile yields in liquid culture of biocontrol nematodes Steinernema carpocapsae and S. feltiae (nematoda: Rhabditida). Applied Microbiology and Biotechnology 85, 507–515.CrossRefGoogle Scholar
Keeling, CI and Bohlmann, J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytologist 170, 657–675.CrossRefGoogle ScholarPubMed
Lewinsohn, E, Gijzen, M and Croteau, R (1991) Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiology 96, 44–49.CrossRefGoogle ScholarPubMed
Linit, M and Stamps, WT (2001) Interaction of intrinsic and extrinsic chemical cues in the behaviour of Bursaphelenchus xylophilus (Aphelenchida: Aphelenchoididae) in relation to its beetle vectors. Nematology 3, 295.CrossRefGoogle Scholar
Maehara, N and Futai, K (2000) Population changes of the pinewood nematode, Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), on fungi growing in pine-branch segments. Applied Entomology and Zoology 35, 413–417.CrossRefGoogle Scholar
Maehara, N and Futai, K (2001) Presence of the cerambycid beetles Psacothea hilaris and Monochamus alternatus affecting the life cycle strategy of Bursaphelenchus xylophilus. Nematology 3, 455.CrossRefGoogle Scholar
Mamiya, Y (1975) The life history of the pine wood nematode, Bursaphelenchus lignicolus. Japanese Journal of Nematology 5, 16–25.Google Scholar
Mamiya, Y (1983 a) The effect of wood tissues on the molting rate of the dauerlarvae of Bursaphelenchus xylophilus. Japanese Journal of Nematology 13, 6–13.Google Scholar
Mamiya, Y (1983 b) Pathology of the pine wilt disease caused by Bursaphelenchus xylophilus. Annual Review of Phytopathology 21, 201–220.CrossRefGoogle ScholarPubMed
Mota, MM, Braasch, H, Bravo, MA, Penas, AC, Burgermeister, W, Metge, K and Sousa, E (1999) First report of Bursaphelenchus xylophilus in Portugal and in Europe. Nematology 1, 727–734.Google Scholar
Murgatroyd, C and Spengler, D (2010) Histone tales: echoes from the past, prospects for the future. Genome Biology 11, 105.CrossRefGoogle ScholarPubMed
Nickle, W, Golden, A, Mamiya, Y and Wergin, W (1981) On the taxonomy and morphology of the pine wood nematode, Bursaphelenchus xylophilus (Steiner & Buhrer 1934) Nickle 1970. Journal of Nematology 13, 385.Google Scholar
Niu, H, Zhao, L, Lu, M, Zhang, S and Sun, J (2012) The ratio and concentration of two monoterpenes mediate fecundity of the pinewood nematode and growth of its associated fungi. PloS One 7, e31716.CrossRefGoogle ScholarPubMed
Ouellet, J, Li, S and Roy, R (2008) Notch signalling is required for both dauer maintenance and recovery in C. elegans. Development 135, 2583–2592.CrossRefGoogle ScholarPubMed
Smith, R (2000) Xylem monoterpenes of pines: distribution, variation, genetics, function. USDA Forest Service General Technical Report 177, 454.Google Scholar
Stamps, WT and Linit, MJ (1995) A rapid and simple method for staining lipid in fixed nematodes. Journal of Nematology 27, 244–248.Google ScholarPubMed
Stamps, WT and Linit, MJ (1998 a) Chemotactic response of propagative and dispersal forms of the pinewood nematode Bursaphelenchus xylophilus to beetle and pine derived compounds. Fundamental and Applied Nematology 21, 243–250.Google Scholar
Stamps, WT and Linit, MJ (1998 b) Neutral storage lipid and exit behavior of Bursaphelenchus xylophilus fourth-stage dispersal juveniles from their beetle vectors. Journal of Nematology 30, 255–261.Google ScholarPubMed
Storey, RMJ (1984) The relationship between neutral lipid reserves and infectivity for hatched and dormant juveniles of Globodera spp. Annals of Applied Biology 104, 511–520.CrossRefGoogle Scholar
Strauch, O and Ehlers, RU (1998) Food signal production of Photorhabdus luminescens inducing the recovery of entomopathogenic nematodes Heterorhabditis spp. in liquid culture. Applied Microbiology and Biotechnology 50, 369–374.CrossRefGoogle Scholar
Su, J-W, Zeng, J-P, Qin, X-W and Ge, F (2008) Effect of needle damage on the release rate of Masson pine (Pinus massoniana) volatiles. Journal of Plant Research 122, 193.CrossRefGoogle ScholarPubMed
Van Gundy, SD (1967) Aging and starvation in larvae of Meloidogyne javanica and Tylenchulus semipenetrans. Phytopathology 57, 559–571.Google Scholar
Xu, L, Lou, Q, Cheng, C, Lu, M and Sun, J (2015) Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production. Microbial Ecology 70, 1012–1023.CrossRefGoogle ScholarPubMed
Xu, L, Shi, Z, Wang, B, Lu, M and Sun, J (2016) Pine defensive monoterpene alpha-pinene influences the feeding behavior of Dendroctonus valens and its gut bacterial community structure. International journal of molecular sciences 17, 1734.CrossRefGoogle ScholarPubMed
Xu, D, Xu, L, Zhou, F, Wang, B, Wang, S, Lu, M and Sun, J (2018) Gut bacterial communities of Dendroctonus valens and monoterpenes and carbohydrates of Pinus tabuliformis at different attack densities to host pines. Frontiers in Microbiology 9, 1251.CrossRefGoogle ScholarPubMed
Yi, CK, Byun, BH, Park, JD, Yang, S and Chang, KH (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 (Seoul) 38, 141–149.Google Scholar
Zamora, P, Rodriguez, V, Renedo, F, Sanz, AV, Dominguez, JC, Perez-Escolar, G, Miranda, J, Alvarez, B, Gonzalez-Casas, A, Mayor, E, Duenas, M, Miravalles, A, Navas, A, Robertson, L and Martin, AB (2015) First report of Bursaphelenchus xylophilus causing pine wilt disease on Pinus radiata in Spain. Plant Disease 99, 1449–1449.CrossRefGoogle Scholar
Zhao, LL, Wei, W, Kang, L and Sun, JH (2007) Chemotaxis of the pinewood nematode, Bursaphelenchus xylophilus, to volatiles associated with host pine, Pinus massoniana, and its vector Monochamus alternatus. Journal of Chemical Ecology 33, 1207–1216.CrossRefGoogle ScholarPubMed
Zhao, LL, Zhang, S, Wei, W, Hao, H, Zhang, B, Butcher, RA and Sun, J (2013) Chemical signals synchronize the life cycles of a plant-parasitic nematode and its vector beetle. Current Biology 23, 2038–2043.CrossRefGoogle ScholarPubMed
Zhao, L, Mota, M, Vieira, P, Butcher, RA and Sun, J (2014) Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends in Parasitology 30, 299–308.CrossRefGoogle ScholarPubMed
Zhao, L, Zhang, X, Wei, Y, Zhou, J, Zhang, W, Qin, P, Chinta, S, Kong, X, Liu, Y, Yu, H, Hu, S, Zou, Z, Butcher, RA and Sun, J (2016) Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle. Nature Communications 7, 12341.CrossRefGoogle ScholarPubMed
Zhou, F, Xu, L, Wang, S, Wang, B, Lou, Q, Lu, M and Sun, J (2017) Bacterial volatile ammonia regulates the consumption sequence of d-pinitol and d-glucose in a fungus associated with an invasive bark beetle. The Isme Journal 11, 2809.CrossRefGoogle Scholar
Supplementary material: PDF

Zhang et al. supplementary material

Table S1
Download Zhang et al. supplementary material(PDF)
PDF 279.6 KB