Skip to main content
SpringerLink
Log in

Ophiostomatales (Ascomycota) associated with Tomicus species in southwestern China with an emphasis on Ophiostoma canum

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Ophiostomatalean fungi may facilitate bark beetle colonization and reproduction. In the present study of the fungal community associated with bark beetle species belonging to Tomicus in Yunnan, China, six ophiostomatalean fungi (Ophiostoma canum, O. ips, O. tingens, Leptographium yunnanense, Leptographium sp. 1 and Leptographium sp. 2) were isolated from the beetles or their galleries; O. canum was the most common fungal species. The distribution of O. canum was associated with stands heavily damaged by Tomicus species and a higher percentage of valid galleries of Tomicus yunnanensis and T. minor in Yunnan pine (Pinus yunnanensis). After inoculation of Yunnan pine with the fungus, a phloem reaction zone formed and monoterpenes accumulated in the phloem. These results suggested that O. canum was pathogenic to Yunnan pine and that the wide distribution of the fungus might be beneficial to reproduction of pine shoot beetles in Yunnan pine. However, because the reaction zone and monoterpene accumulation were mild, fungal damage of Yunnan pine might be limited. A more integrated study considering all the fungal species should be done to better understand the interactions among bark beetles, blue-stain fungi, and the tree hosts in the region.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alamouti SM, Tsui CKM, Breuil C (2009) Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycol Res 113(8):822–835

    CAS  Google Scholar 

  • Batra LR (1967) Ambrosia fungi: a taxonomic revision, and nutritional studies of some species. Mycologia 59(6):976–1017

    Google Scholar 

  • Bordasch RP, Berryman AA (1977) Host resistance to the fir engraver beetle, Scolytus ventralis (Coleoptera: Scolytidae): 2. Repellency of Abies grandis resins and some monoterpenes. Can Entomol 109(1):95–100

    CAS  Google Scholar 

  • Bruno JF, Satchowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18(3):119–125

    Google Scholar 

  • Chang RL, Duong TA, Taerum SJ, Wingfield MJ, Zhou XD, De Beer ZW (2017) Ophiostomatoid fungi associated with conifer-infesting beetles and their phoretic mites in Yunnan, China. MycoKeys 28(28):19–64

    Google Scholar 

  • Chen P (2011) The population quantity and spatial distribution characteristics of Tomicus yunnanensis. In: Ye H, Lu J, Chen P, Duan YQ, Liao ZY (eds) Tomicus yunnanensis. Yunnan Science and Technology Press, Yunnan Publishing Group, Kunming, pp 32–45

    Google Scholar 

  • Davydenko K, Vasaitis R, MeshkovaV Menkis A (2014) Fungi associated with the red-haired bark beetle, Hylurgus ligniperda (coleoptera: curculionidae) in the forest-steppe zone in eastern Ukraine. Eur J Entomol 111:561–565

    Google Scholar 

  • De Beer ZW, Wingfield MJ (2013) Emerging lineages in the Ophiostomatales. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) The ophiostomatoid fungi: expanding frontiers. CBS biodiversity series. CBS-KNAW Fungal Biodiversity Centre, Utrecht, pp 21–46

    Google Scholar 

  • De Beer ZW, Duong TA, Wingfield MJ (2016) The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 83:165–191

    PubMed  PubMed Central  Google Scholar 

  • Delorme L, Lieutier F (1990) Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi. For Pathol 20(5):304–316

    Google Scholar 

  • Duan YQ (2011) The damage characteristics of Tomicus yunanensis. In: Ye H, Lu J, Chen L, Duan YQ, Liao ZY (eds) Tomicus yunnanensis. Yunnan Science and Technology Press, Yunnan Publishing Group, Kunming, pp 46–67

    Google Scholar 

  • Fäldt J, Solheim H, Långström B, Borg-Karlson AK (2006) Influence of fungal infection and wounding on contents and enantiomeric compositions of monoterpenes in phloem of Pinus sylvestris. J Chem Ecol 32(8):1779–1795

    PubMed  Google Scholar 

  • Francke-Grosmann H (1952) Über die Ambrosiazucht der beiden Kiefernborkenkäfer Mycelo-philus minor Htg. und Ips acuminatus Gyll. Meddelanden Från Statens Skogsforsknings-institute 41:1–52

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gershenzon J, Croteau R (1991) Terpenoids. In: Rosenthal GA, Berenbaum MR (eds) Herbivores, their interactions with secondary plant metabolites. Academic Press, San Diego, pp 165–219

    Google Scholar 

  • Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3(7):408–414

    CAS  PubMed  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microb 61(4):1323–1330

    CAS  Google Scholar 

  • Goldazarena A, Romón P, López S (2012) Bark beetles control in forests of Northern Spain. In: Larramendy ML, Soloneski S (eds) Integrated pest management and pest control-current and future tactics. Janeza Trdine, Croatia, pp 323–352

    Google Scholar 

  • Grobbelaar JW, Aghayeva D, De Beer ZW, Bloomer P, Wingfield MJ, Wingfield BD (2009) Delimitation of Ophiostoma quercus and its synonyms using multiple gene phylogenies. Mycol Prog 8(3):221–236

    Google Scholar 

  • Harrington TC, Aghayeva DN, Fraedrich SW (2010) New combinations in Raffaelea, Ambrosiella, and Hyalorhinocladiella, and four new species from the redbay ambrosia beetle, Xyleborus glabratus. Mycotaxon 111(1):337–361

    Google Scholar 

  • He DM, Zhang FQ (2004) Disaster and control for Tomicus beetles in Yunnan province. For Inventory Plan 29:251–252

    Google Scholar 

  • Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, Wingfield BD (2004) Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol Res 108(4):411–418

    PubMed  Google Scholar 

  • Jacobs K, Eckhardt LG, Wingfield MJ (2006) Leptographium profanum sp. nov., a new species from hardwood roots in North America. Botany 84(5):759–766

    Google Scholar 

  • Jankowiak R (2008) Fungi associated with Tomicus minor on Pinus sylvestris in Poland and their succession into the sapwood of beetle-infested windblown trees. Can J For Res 38(38):2579–2588

    Google Scholar 

  • Jankowiak R (2012) Ophiostomatoid fungi associated with Ips sexdentatus on Pinus sylvestris in Poland. Dendrobiology 68(1):43–54

    Google Scholar 

  • Jankowiak R, Bilanski P (2007) Fungal flora associated with Tomicus piniperda L. in an area close to a timber yard in southern Poland. J Appl Entomol 131(8):579–584

    Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23(10):403–405

    CAS  PubMed  Google Scholar 

  • Joseph LM, Koon TT, Man WS (1998) Antifungal effects of hydrogen peroxide and peroxidase on spore germination and mycelial growth of Pseudocercospora species. Can J Bot 76(76):2119–2124

    CAS  Google Scholar 

  • Krokene P, Solheim H (1999) What do low-density inoculations with fungus tell us about fungal virulence and tree resistance? In: Lieutier F, Mattson WJ, Wagner MR (eds) Physiology and genetics of tree-phytophage interactions. International symposium, Gujan (France) August 31–September 5, 1997. INRA, Les Colloques 90, pp 353–362

  • Lanne BS, Schlyter F, Byers JA, Löfqvist J, Leufvén A, Bergström G, Van der Pers JN, Unelius R, Baeckström P, Norin T (1987) Differences in attraction to semiochemicals present in sympatric pine shoot beetles, Tomicus minor and T. piniperda. J Chem Ecol 13(5):1045–1067

    CAS  PubMed  Google Scholar 

  • Li LS, Cai XS, Wang HL, Yang DS (1997) Study on relationship between damage of Tomicus piniperda and its environment. Yunnan For Sci Technol 2:8–13

    Google Scholar 

  • Liao ZY, Ye H (2002) Pathogenic mechanisms of Leptographium yunnanense, a fungus associated with Tomicus piniperda L. For Pest Dis 21(3):3–5

    Google Scholar 

  • Liao ZY, Ye H (2004) Action mechanisms of phytotoxin produced by Leptographium yunnanense associated with Tomicus piniperda. For Pest Dis 23(1):20–22

    Google Scholar 

  • Lieutier F, Yart A, Salle A (2009) Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci 66(8):801

    Google Scholar 

  • Linnakoski R, De Beer ZW, Ahtiainen J, Sidorov E, Niemelä P, Pappinen A, Wingfield MJ (2010) Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. Persoonia 25(1):72–93

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu J (2011) The identification characteristics of Tomicus yunanensis. In: Ye H, Lu J, Chen P, Duan YQ, Liao ZY (eds) Tomicus yunnanensis Yunnan science and Technology Press. Yunnan Publishing Group, Kunming, pp 1–14

    Google Scholar 

  • Masuya H, Kaneko S, Yamaoka Y, Osawa M (1999) Comparisons of Ophiostomatoid fungi associated and T. minor in Japanese red pine. J For Res Jpn 4(2):131–135

    Google Scholar 

  • Masuya H, Kaneko S, Yamaoka Y (2003) Comparative virulence of blue-stain fungi isolated from Japanese red pine. J Forest Res-Jpn 8(2):83–88

    Google Scholar 

  • Mathiesen A (1950) Über einige mit Borkenkäfern assoziierte Bläuepilze in Schweden. Oikos 2:275–308

    Google Scholar 

  • Mathiesen-Käärik A (1953) Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläuepilze. Meddelanden Från Statens Skogsforskningsinstitut 43:1–74

    Google Scholar 

  • Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol S 36(36):563–595

    Google Scholar 

  • Münch E (1907) De Blaufäule des Nadelholzes. I-II. Naturwissenschaftliche Zeitschrift für Forst- und Landwirtschaft 5:531–573

    Google Scholar 

  • Paciura D, De Beer ZW, Jacobs K, Ye H, Zhou XD, Wingfield MJ (2010) Eight new Leptographium species associated with tree-infesting bark beetles in China. Persoonia 25(6):94–108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Y (2018) Diversity, colonization ability and roles of fungi associated with Tomicus spp. during the Tomicus damage in Southwestern China. Doctoral thesis. Yunnan University, Kunming

  • Pan Y, Chen P, Lu J, Zhou XD, Ye H (2017) First report of blue-stain in Pinus Yunnanensis caused by Ophiostoma tingens associated with Tomicus minor in China. J Plant Pathol 99(3):805

    Google Scholar 

  • Pan Y, Lu J, Zhou XD, Chen P, Zhang HH, Ye H (2018a) Leptographium wushanense sp. nov., associated with Tomicus armandii on Pinus armandii in Southwestern China. Mycoscience. https://doi.org/10.1016/j.myc.2018.10.003

    Article  Google Scholar 

  • Pan Y, Zhao T, Krokene P, Yu ZF, Qiao M, Lu J, Chen P, Ye H (2018b) Beetle-associated blue-stain fungi increase antioxidant enzyme activities and monoterpene concentrations in Pinus yunnanensis. Front Plant Sci 9:1731–1740

    PubMed  PubMed Central  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    CAS  PubMed  Google Scholar 

  • Raffa KF, Berryman AA (1982) Accumulation of monoterpenes and associated volatiles following inoculation of grand fir with a fungus transmitted by the fir engraver, Scolytus ventralis (Coleoptera: Scolytidae). Can Entomol 114(9):797–810

    CAS  Google Scholar 

  • Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in conifer defense against bark beetle-microbial complexes. Oecologia 102(3):285–295

    PubMed  Google Scholar 

  • Rennerfelt E (1950) Über den Zusammenhang zwischen dem Verblauen des Holzes und den Insekten. Oikos 2:120–137

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  PubMed  Google Scholar 

  • Sapp J (1994) Evolution by association: a history of symbiosis. Oxford University Press, New York

    Google Scholar 

  • Seifert KA (1993) Sapstain of commercial lumber by species of Ophiostma and Ceratocystis. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and Ophiostoma. Taxonomy, ecology and pathogenicity. American Phytopathological Press, St. Paul, pp 141–151

    Google Scholar 

  • Six DL (2012) Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects 3(1):339–366

    PubMed  PubMed Central  Google Scholar 

  • Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol 56(1):255–272

    CAS  PubMed  Google Scholar 

  • Solheim H, Krokene P, Långström B (2001) Effects of growth and virulence of associated blue-stain fungi on host colonization behaviour of the pine shoot beetles Tomicus minor and T. piniperda. Plant Pathol 50:111–116

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viiri H, Annila E, Kitunen V, Niemelä P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with bluestain fungus, Ceratocystis polonica. Trees Struct Funct 15:112–122

    CAS  Google Scholar 

  • Wang X, Wang TT, Wang JC, Guan TL, Li HM (2014) Morphological, molecular and biological characterization of Esteya vermicola, a nematophagous fungus isolated from intercepted wood packing materials exported from Brazil. Mycoscience 55(5):367–377

    Google Scholar 

  • Wang XW, Chen P, Wang YX, Yuan RL, Feng D, Li LS, Ye H, Pan Y, Lu J, Zhou YF, Du CH (2018) Population structure and succession law of Tomicus species in Yunnan. For Res 31(3):167–172

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of ungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Zhang X (2001) Thinking of Tomicus beetles control in Yunnan Province. For Pest Dis 20:42–44

    Google Scholar 

  • Zhao T, Solheim H, Långström B, Borg-Karlson AK (2011) Storm-induced tree resistance and chemical differences in Norway spruce (Picea abies). Ann For Sci 68(3):657–665

    Google Scholar 

  • Zhao T, Axelsson K, Krokene P, Borg-Karlson AK (2015) Fungal symbionts of the spruce bark beetle synthesize the beetle aggregation pheromone 2-methyl-3-buten-2-ol. J Chem Ecol 41(9):848–852

    CAS  PubMed  Google Scholar 

  • Zhao T, Ganji S, Schiebe C, Bohman B, Weinstein P, Krokene P, Borg-Karlson AK, Unelisu R (2019) Convergent evolution of semiochemicals across Kingdoms: bark beetles and their fungal symbionts. ISME J. https://doi.org/10.1038/s41396-019-0370-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou XD, Jacobs K, Morelet M, Ye H, Lieutier F, Wingfield MJ (2000) A new Leptographium species associated with Tomicus piniperda in south-western China. Mycoscience 41(6):573–578

    Google Scholar 

  • Zhou XD, Burgess TI, De Beer ZW, Lieutier F, Yart A, Klepzig K, Carnegie A, Portales MP, Wingfield BD, Wingfield MJ (2007) High intercontinental migration rates and population admixture in the sapstain fungus Ophiostoma ips. Mol Ecol 16(1):89–99

    CAS  PubMed  Google Scholar 

  • Zhou XD, De Beer ZW, Wingfield MJ (2013) Ophiostomatoid fungi associated with conifer-infesting bark beetles in China. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) The Ophiostomatoid Fungi: expanding frontiers. CBS biodiversity series. CBS-KNAW Fungal Biodiversity Centre, Utrecht, pp 91–98

    Google Scholar 

  • Zhou XD, Burgess T, De Beer ZW, Wingfield BD, Wingfield MJ (2015) Development of polymorphic microsatellite markers for the tree pathogen and sapstain agent, Ophiostoma ips. Mol Ecol Notes 2(3):309–312

    Google Scholar 

  • Zipfel RD, De Beer ZW, Jacobs K, Wingfield BD, Wingfield MJ (2006) Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud Mycol 55(55):75–97

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Eco-development Academy, Southwest Forestry University, Kunming, 650224, People’s Republic of China

    Yue Pan

  2. Laboratory of Biological Invasion and Ecosecurity, Yunnan University, Kunming, 650091, People’s Republic of China

    Yue Pan, Jun Lu, Huihong Zhang & Hui Ye

  3. Yunnan Academy of Forestry and Grassland, Kunming, 650201, People’s Republic of China

    Peng Chen

  4. Laboratory for Conservation and Utilization of Bio-resources, Key Laboratory Resources of the Ministry of Education, Yunnan University, Kunming, 650091, People’s Republic of China

    Zefen Yu

  5. Department of Science and Technology, Örebro University, 701 82, Örebro, Sweden

    Tao Zhao

Authors
  1. Yue Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zefen Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huihong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hui Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hui Ye or Tao Zhao.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: The work was supported by the Natural Science Foundation of China (No. 31360183), the Applied Basic Research Foundation of Yunnan Province (No. 2013FA055), National Key R&D Program of China (2017YFC0505206) and Swedish Research Council FORMAS and Örebro University.

The online version is available at http://www.springerlink.com

Corresponding editor: Tao Xu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, Y., Lu, J., Chen, P. et al. Ophiostomatales (Ascomycota) associated with Tomicus species in southwestern China with an emphasis on Ophiostoma canum. J. For. Res. 31, 2549–2562 (2020). https://doi.org/10.1007/s11676-019-01029-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-019-01029-1

Keywords

Search

Navigation