Skip to main content
SpringerLink
Log in

Effect of ectomycorrhizal composition on survival and growth of Pinus thunbergii seedlings varying in resistance to the pine wilt nematode

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Ectomycorrhizal composition and associated fungi affect the intra-specific ability of resistant black pines for physiological adaptation.

Abstract

Since Japanese black pine (Pinus thunbergii Parl.) forests have been widely devastated by pine wilt disease, several kinds of resistant black pines have been developed. Although all of the resistant black pines are the same species, these resistant trees show different physiological characteristics. We investigated the survival rates and growth rates, as well as ectomycorrhizal composition and associated fungi, on four kinds of Japanese black pine seedlings (three pine wilt-resistant and one non-resistant), and elucidated the factors affecting the various physiological characteristics. We found that the abundance of ectomycorrhizal types differed even though seedlings were grown sympatrically in the same areas for about 2 years. The seedlings that had plentiful white ectomycorrhizae showed the highest survival and growth rates regardless of the variety of black pine. Sequence similarities of the white ectomycorrhizae in the rDNA ITS region were best matched with members of Astraeus sp., Atheliaceae, Boletaceae and Thelephoraceae. Our findings indicate that intra-specific physiological adaptation might be affected by ectomycorrhizal composition or by the specific ectomycorrhizal species.

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
Fig. 4

Similar content being viewed by others

References

  • Aggangan NS, Aggangan JS, Bulan JCO, Limos CAS (2012) Inoculation of dipterocarps Anisoptera thurifera and Shorea guiso with ectomycorrhizal fungi in Philippine red soil. Philipp J Sci 14:229–241

    Google Scholar 

  • Akema T, Futai K (2005) Ectomycorrhizal development in Pinus thunbergii stand in relation to location on a slope and effect on tree mortality from pine wilt disease. J For Res 10:93–99

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bledsoe CS (1992) Physiological ecology of ectomycorrhizae: implications for field application. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman Hall, New York

    Google Scholar 

  • Buscot F, Weber G, Obervinkler F (1992) Interactions between Cylindrocarpon destructans and ectomycorrhizas of Picea abies with Laccaria laccata and Paxillus involutus. Trees 6:83–90

    Article  Google Scholar 

  • Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836

    Article  Google Scholar 

  • Faraway JJ (2006) Random effects. In: Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models, CRC Press, Boca, Raton, pp 153––183

  • Fernandez CW, Koide RT (2013) The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecol 6:479–486

    Article  Google Scholar 

  • Finlay RD, Read DJ (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The uptake and distribution of phosphorus by mycelial strands interconnecting host plants. New Phytol 103:157–165

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Johnson D (2015) Priorities for research on priority effects. New Phytol 205:1375–1377

    Article  PubMed  Google Scholar 

  • Johnson D, Martin F, Cairney JWG, Anderson IC (2012) The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol 194:614–628

    Article  PubMed  Google Scholar 

  • Kaewgrajang T, Sangwanit U, Iwase K, Kodama M, Yamato M (2013) Effects of ectomycorrhizal fungus Astraeus odoratus on Dipterocarpus alatus seedlings. J Trop For Sci 25:200–205

    Google Scholar 

  • Kayama M, Yamanaka T (2014) Growth characteristics of ectomycorrhizal seedlings of Quercus glauca, Quercus salicina, and Castanopsis cuspidata planted on acidic soil. Trees 28:569–583

    Article  CAS  Google Scholar 

  • Kikuchi J, Tsuno N, Futai K (1991) The effect of mycorrhizae as a resistance factor of pine trees to the pinewood menatode (in Japanese with English summary). J Jpn For Soc 73:216–218

    Google Scholar 

  • Kishi Y (1995) The pine wood nematode and the Japanese pine sawyer. Thomas, Tokyo

    Google Scholar 

  • Kishi Y (1999) Influence of tree age on wilt and mortality of pines after inoculation with Bursaphelenchus xylophilus (in Japanese with English summary). J Jpn For Soc 81:330–333

    Google Scholar 

  • Kobayashi F, Yamane A, Ikeda T (1984) The Japanese pine sawyer beetle as the vector of pine wilt disease. Annu Rev Ent 29:115–135

    Article  Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Matsuda Y, Noguchi Y, Ito S (2009) Ectomycorrhizal fungal community of naturally regenerated Pinus thunbergii seedlings in a coastal pine forest. J For Res 14:335–341

    Article  CAS  Google Scholar 

  • Matsuda Y, Takano Y, Shimada H, Yamanaka T, Ito S (2013) Distribution of ectomycorrhizal fungi in a Chamaecyparis obtusa stand at different distances from a mature Quercus serrata tree. Mycoscience 54:260–264

    Article  Google Scholar 

  • Obase K, Lee JK, Lee SY, Chun KW (2011) Diversity and community structure of ectomycorrhizal fungi in Pinus thunbergii forests in the eastern region of Korea. Mycoscience 52:383–391

    Article  Google Scholar 

  • Ohigashi K (2010) An introductory guide to the statistical analysis—from general linear model to the generalized linear model—(in Japanese). J Weed Sci Tech 55:268–274

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available online at http://www.r-project.org/. Accessed 19 Dec 2013

  • Sarjala T, Niemi K, Häggman H (2010) Mycorrhiza formation is not needed for early growth induction and growth-related changes in polyamines in Scots pine seedlings in vitro. Plant Physiol Biochem 48:596–601

    Article  CAS  PubMed  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf A et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taniguchi T, Kanzaki N, Tamai S, Yamanaka N, Futai K (2007) Does ectomycorrhizal fungal community structure vary along a Japanese black pine (Pinus thunbergii) to black locust (Robinia pseudoacacia) gradient? New Phytol 173:322–334

    Article  PubMed  Google Scholar 

  • Toda T (2004) Studies on the breeding for resistance to the pine wilt disease in Pinus densiflora and P. thunbergii (in Japanese). Bull For Tree Breed Center 20:83–217

    Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    Article  PubMed  Google Scholar 

Download references

Author contribution statement

HN conceived of the study, carried out the field survey, participated in the DNA analysis, performed the statistical analysis and drafted the manuscript. NE carried out the field survey and helped to draft the manuscript. TU played a central role in the DNA analysis. NY carried out the field survey and participated in the coordination of this study. YM played an extraordinary role in conception and design of this study, and helped to draft the manuscript. All authors read and approved the final manuscript.

Acknowledgments

We thank the editor and two anonymous reviewers for their valuable comments on the draft manuscript. We also thank Dr. Akira Ishida, Mr. Yusuke Ogasawara, Mr. Yusuke Uehara, Ms. Nobumi Toyoda, and all the members of Aichi Prefectural Forestry Research Institute, Aichi Prefectural Mariculture Center, and the Forest Pathology and Mycology Laboratory, Graduate School of Bioresources, Mie University, for their help during our study, and Ms. Tomiko Chikada, the Mie University Life Science Research Center for DNA sequencing. This study was supported in part by the Grants-in-Aid for Scientific Research from the Japan Ministry of Education, Science, Sports and Culture to YM (25304026).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Aichi Prefectural Forestry Research Institute, 43-1 Kamiyoshida, Otsuarata, Shinshiro, Aichi, 441-1622, Japan

    Hirofumi Nakashima, Norikazu Eguchi & Noboru Yamashita

  2. Laboratory of Forest Pathology and Mycology, Graduate School of Bioresources, Mie University, 1577 Kurimamachiya, Tsu, Mie, 514-8105, Japan

    Takashi Uesugi & Yosuke Matsuda

Authors
  1. Hirofumi Nakashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norikazu Eguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Uesugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noboru Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yosuke Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hirofumi Nakashima.

Additional information

Communicated by T. Koike and K. Noguchi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3833 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakashima, H., Eguchi, N., Uesugi, T. et al. Effect of ectomycorrhizal composition on survival and growth of Pinus thunbergii seedlings varying in resistance to the pine wilt nematode. Trees 30, 475–481 (2016). https://doi.org/10.1007/s00468-015-1217-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-015-1217-0

Keywords

Search

Navigation