Skip to main content
SpringerLink
Log in

Feasibility analysis of Arabidopsis thaliana as an alternative host for research on interactions of pinewood nematodes with plants

  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

Bursaphelenchus xylophilus causes pine wilt disease and substantial economic losses. However, as Pinus has some limitations as a host for studies, information about the interactions between B. xylophilus and Pinus at the molecular level is limited. The use of an alternative plant would greatly facilitate a better understanding of the plant-nematode interactions. In this study, we explored the feasibility of Arabidopsis thaliana as an alternative host to investigate the relationship between plants and B. xylophilus and established a system for the efficient infection of A. thaliana by B. xylophilus (defined in this paper as the mean number of plants infested with B. xylophilus) by evaluating the artificial wounding of seedlings, ages of seedlings and nematode inoculum concentrations, and then the susceptibility of nine A. thaliana ecotypes was tested. The results showed that B. xylophilus infected all ecotypes tested. Artificially wounding the petiole of the first leaf increased the plant infection rate of B. xylophilus, reaching 90 % of the inoculated plants with inoculum concentration of 400 nematodes per plant at 15 days after germination (DAG). A typical symptom was yellowing of the entire plant and browning of older leaves 72 h after inoculation. Membrane damage of the thylakoid lamellae, collapse of chloroplasts and increase of the electron density of the cytoplasm were also observed. Our results demonstrated that B. xylophilus could invade Arabidopsis and cause similar early symptoms to that of pine trees, yet B. xylophilus could not reproduce in A. thaliana. Nonetheless, A. thaliana may be used to study the early response of plants to B. xylophilus and it provides a new opportunity for studying B. xylophilus-plant interactions.

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

Similar content being viewed by others

References

  • Ahuja MR, Neale DB (2005) Evolution of genome size in conifers. Silvae Genetica 54(3):126–137

    Google Scholar 

  • Baum TJ, Wubben MJ, Hardyy KA, Su H, Rodermel SR (2000) A screen for Arabidopsis thaliana mutants with altered susceptibility to Heterodera schachtii. J Nematol 32(2):166–173

    PubMed  CAS  Google Scholar 

  • Boiteux LS, Fonseca MEN, Simon PW (1999) Host status and reaction of Arabidopsis thaliana ecotypes to infection by the northern root-knot nematode (Meloidogyne hapla). Plant Breed 118(4):355–358

    Article  Google Scholar 

  • Byun YC, Park B, Yang S (1989) First finding of the pine wood nematode, Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle and its insect vector in Korea. Res Rep Forest Res Inst Seoul 38:141–149

    Google Scholar 

  • Cheng H, Lin M, Li W, Fang Z (1983) The occurrence of a pine wilting disease caused by nematode found in Nanjing. Forest Pest Dis 4:1–5

    Google Scholar 

  • Eckert AJ, Pande B, Ersoz ES, Wright MH, Rashbrook VK, Nicolet CM, Neale DB (2009) High-throughput genotyping and mapping of single nucleotide polymorphisms in loblolly pine (Pinus taeda L.). Tree Genet Genome 5(1):225–234

    Article  Google Scholar 

  • Elsen A, Lens K, Nguyet DTM, Broos S, Stoffelen R, De Waele D (2001) Aseptic culture systems of Radopholus similis for in vitro assays on Musa spp. and Arabidopsis thaliana. J Nematol 33(2–3):147–151

    PubMed  CAS  Google Scholar 

  • Fukuda K (1997) Physiological process of the symptom development and resistance mechanism in pine wilt disease. J For Res 2(3):171–181

    Article  Google Scholar 

  • Gion JM, Lalanne C et al (2005) The proteome of maritime pine wood forming tissue. Proteomics 5(14):3731–3751

    Article  PubMed  CAS  Google Scholar 

  • Grundler FMW, Sobczak M, Lange S (1997) Defence responses of Arabidopsis thaliana during invasion and feeding site induction by the plant–parasitic nematode Heterodera glycines. Physiol Mol Plant Pathol 50(6):419–430

    Article  Google Scholar 

  • Hirao T, Fukatsu E, Watanabe A (2012) Characterization of resistance to pine wood nematode infection in Pinus thunbergii using suppression subtractive hybridization. BMC Plant Biol 12(1):13. doi:10.1186/1471-2229-12-13

    Article  PubMed  CAS  Google Scholar 

  • Huala E, Dickerman AW et al (2001) The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 29(1):102–105

    Article  PubMed  CAS  Google Scholar 

  • Ichihara Y, Fukuda K, Suzuki K (2000) Early symptom development and histological changes associated with migration of Bursaphelenchus xylophilus in seedling tissues of Pinus thunbergii. Plant Dis 84(6):675–680

    Article  Google Scholar 

  • Jones JT, Moens M, Mota M, Li HM, Kikuchi T (2008) Bursaphelenchus xylophilus: opportunities in comparative genomics and molecular host-parasite interactions. Mol Plant Pathol 9(3):357–368

    Article  PubMed  Google Scholar 

  • Kikuchi T, Jones JT, Aikawa T, Kosaka H, Ogura N (2004) A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett 572(1–3):201–205

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi T, Shibuya H, Jones JT (2005) Molecular and biochemical characterization of an endo-beta-1,3-glucanase from the pinewood nematode Bursaphelenchus xylophilus acquired by horizontal gene transfer from bacteria. Biochem J 389(Pt 1):117–125

    PubMed  CAS  Google Scholar 

  • Kikuchi T, Shibuya H, Aikawa T, Jones JT (2006) Cloning and characterization of pectate lyases expressed in the esophageal gland of the pine wood nematode Bursaphelenchus xylophilus. Mol Plant-Microbe Interact 19(3):280–287

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi T, Li H, Karim N, Kennedy MW, Moens M, Jones JT, Li HM (2009) Identification of putative expansin-like genes from the pine wood nematode, Bursaphelenchus xylophilus, and evolution of the expansin gene family within the Nematoda. Nematology 11(3):355–364

    Article  CAS  Google Scholar 

  • Lin S, Jian H, Zhao H, Yang D, Liu Q (2011) Cloning and characterization of a venom allergen-like protein gene cluster from the pinewood nematode Bursaphelenchus xylophilus. Exp Parasitol 127(2):440–447

    Article  PubMed  CAS  Google Scholar 

  • Mamiya Y (1983) Pathology of the pine wilt disease caused by Bursaphelenchus xylophilus. Annu Rev Phytopathol 21:201–220

    Article  Google Scholar 

  • Mamiya Y (1988) History of pine wilt disease in Japan. J Nematol 20(2):219–226

    PubMed  CAS  Google Scholar 

  • Mamiya Y (2008) Movement of the pinewood nematode, Bursaphelenchus xylophilus, through tracheids in diseased pine trees. Jpn J Nematol 38(1):41–44

    Article  Google Scholar 

  • Mamiya Y, Enda N (1979) Bursaphelenchus mucronatus n. sp. (Nematoda, Aphelenchoidadae) from pine wood and its biology and pathogenicity to pine trees. Nematologica 25(3):353–361

    Article  Google Scholar 

  • Mota MM, Braasch H, Bravo MA, Penas AC, Burgermeister W, Metge K, Sousa E (1999) First report of Bursaphelenchus xylophilus in Portugal and in Europe. Nematology 1:727–734

    Article  Google Scholar 

  • Myers RF (1988) Pathogenesis in pine wilt caused by pinewood nematode, Bursaphelenchus xylophilus. J Nematol 20(2):236–244

    PubMed  CAS  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9(7):325–330

    Article  PubMed  CAS  Google Scholar 

  • Nose M, Shiraishi S (2011) Comparison of the gene expression profiles of resistant and non-resistant Japanese black pine inoculated with pine wood nematode using a modified LongSAGE technique. For Pathol 41(2):143–155

    Article  Google Scholar 

  • Plomion C, Cooke J, Richardson T, Mackay J, Tuskan G (2003) Report on the forest trees workshop at the plant and animal genome conference. Comp Func Genom 4(2):229–238

    Article  CAS  Google Scholar 

  • Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33(5):911–921

    Article  PubMed  CAS  Google Scholar 

  • Puzio PS, Lausen J, Almeida-Engler J, Cai DG, Gheysen G, Grundler FMW (1999) Isolation of a gene from Arabidopsis thaliana related to nematode feeding structures. Gene 239(1):163–172

    Article  PubMed  CAS  Google Scholar 

  • Shin H, Lee H, Woo KS, Noh EW, Koo YB, Lee KJ (2009) Identification of genes upregulated by pinewood nematode inoculation in Japanese red pine. Tree Physiol 29(3):411–421

    Article  PubMed  CAS  Google Scholar 

  • Sijmons PC, Grundler FMW, Vonmende N, Burrows PR, Wyss U (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J 1(2):245–254

    Article  Google Scholar 

  • Sobczak M, Golinowski W, Grundler FMW (1997) Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur J Plant Pathol 103(2):113–124

    Article  Google Scholar 

  • Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil DP, Sykacek P, Grundler FMW, Bohlmann H (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57(5):771–784

    Article  PubMed  CAS  Google Scholar 

  • Tan JJ, Ye JR, Wu XQ, Zhu YF, Li Y (2005) A study on disease development and early diagnosis of pine wood nematode, Bursaphelenchus xylophilus, infection of Japanese black pine. Nematology 7:481–485

    Article  Google Scholar 

  • Togashi K, Jikumaru S (2007) Evolutionary change in a pine wilt system following the invasion of Japan by the pinewood nematode, Bursaphelenchus xylophilus. Ecol Res 22(6):862–868

    Article  Google Scholar 

  • Valvekens D, Vanmontagu M, Vanlijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using Kanamycin selection. Proc Natl Acad Sci U S A 85(15):5536–5540

    Article  PubMed  CAS  Google Scholar 

  • Watanabe A, Isoda K, Ozawa H (Eds) (2007) Isolation of genes expressed in Japanese black pine infected with pine wilt disease. In: Plant & Animal Genomes XV Conference, San Diego, p 501

  • Wyss U, Grundler FMW (1992) Heterodera schachtii and Arabidopsis thaliana, a model host-parasite interaction. Nematologica 38(4):488–493

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Zhizhong Gong (College of Biological Sciences, China Agricultural University) and Prof. Jingao Dong (Agricultural University of Hebei, China) for supplying the Arabidopsis ecotypes. This research was supported by Program for Changjiang Scholars and Innovative Research Team in University (IRT1042), Specialized Research Fund for the Doctoral Program of Higher Education of China (20090008120022), and the Natural Science Foundations of China (Grant Nos. 31000885 and 30670278).

Author information

Authors and Affiliations

  1. Department of Plant Pathology, China Agricultural University, Beijing, 100193, China

    Hai-juan Zhao, Heng Jian, Shu-sen Liu, Quan-xin Guo & Qian Liu

Authors
  1. Hai-juan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shu-sen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Quan-xin Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heng Jian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, Hj., Jian, H., Liu, Ss. et al. Feasibility analysis of Arabidopsis thaliana as an alternative host for research on interactions of pinewood nematodes with plants. Australasian Plant Pathol. 42, 17–25 (2013). https://doi.org/10.1007/s13313-012-0175-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-012-0175-x

Keywords

Search

Navigation