Skip to main content

Advertisement

Log in

Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa

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

Abstract

Introduction of exotic plants change soil microbial communities which may have detrimental ecological consequences for ecosystems. In this study, we examined the community structure and species richness of ectomycorrhizal (EcM) fungi associated with exotic pine plantations in relation to adjacent native ectomycorrhizal trees in Iran to elucidate the symbiont exchange between distantly related hosts, i.e. Fagales (Fagaceae and Betulaceae) and Pinaceae. The combination of morphological and molecular identification approaches revealed that 84.6 % of species with more than one occurrence (at least once on pines) were shared with native trees and only 5.9 % were found exclusively on pine root tips. The community diversity of ectomycorrhizal fungi in the pine plantations adjacent to native EcM trees was comparable to their adjacent native trees, but the isolated plantations hosted relatively a species-poor community. Specific mycobionts of conifers were dominant in the isolated plantation while rarely found in the plantations adjacent to native EcM trees. These data demonstrate the importance of habitat isolation and dispersal limitation of EcM fungi in their potential of host range expansion. The great number of shared and possibly compatible symbiotic species between exotic Pinaceae and local Fagales (Fagaceae and Betulaceae) may reflect their evolutionary adaptations and/or ancestral compatibility with one another.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Koljalg U (2010a) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285

    Article  PubMed  Google Scholar 

  • Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, Parmasto E, Prous M, Aan A, Ots M, Kurina O, Ostonen I, Jõgeva J, Halapuu S, Põldmaa K, Toots M, Truu J, Larsson K-H, Kõljalg U (2010b) PlutoF—a web based workbench for ecological and taxonomic research with an online implementation for fungal ITS sequences. Evol Bioinforma 6:189–196

    Google Scholar 

  • Akhani H, Djamali M, Ghorbanalizadeh A, Ramezani E (2010) Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. Pak J Bot 42:231–258

    Google Scholar 

  • Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354

    Article  PubMed  Google Scholar 

  • Bahram M, Põlme S, Kõljalg U, Tedersoo L (2011) A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi. FEMS Microbiol Ecol 75:313–320

    Article  PubMed  CAS  Google Scholar 

  • Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193:465–473

    Article  PubMed  Google Scholar 

  • Barroetaveña C, Cázares E, Rajchenberg M (2007) Ectomycorrhizal fungi associated with ponderosa pine and Douglas-fir: a comparison of species richness in native western North American forests and Patagonian plantations from Argentina. Mycorrhiza 17:355–373

    Article  PubMed  Google Scholar 

  • Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration. Springer Verlag, Berlin

    Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • Cairney JWG (2000) Evolution of mycorrhiza systems. Naturwissenschaften 87:467–475

    Article  PubMed  CAS  Google Scholar 

  • Chapela IH, Osher LJ, Horton TR, Henn MR (2001) Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biol Biochem 33:1733–1740

    Article  CAS  Google Scholar 

  • Chen YL, Liu S, Dell B (2007) Mycorrhizal status of Eucalyptus plantations in south China and implications for management. Mycorrhiza 17:527–535

    Article  PubMed  Google Scholar 

  • Colwell R (2006) EstimateS: Statistical estimation of species richness and shared species from samples, version 8.0. http://purl.oclc.org/estimates. Accessed 20 July 2009

  • Dickie IA, Bolstridge N, Cooper JA, Peltzer DA (2010) Co–invasion by Pinus and its mycorrhizal fungi. New Phytol 187:475–484

    Article  PubMed  Google Scholar 

  • Díez J, Anta B, Manjón JL, Honrubia M (2001) Genetic variability of Pisolithus isolates associated with native hosts and exotic eucalyptus in the western Mediterranean region. New Phytol 149:577–587

    Article  Google Scholar 

  • Dunstan WA, Dell B, Malajczuk N (1998) The diversity of ectomycorrhizal fungi associated with introduced Pinus spp. in the Southern Hemisphere, with particular reference to Western Australia. Mycorrhiza 8:71–79

    Article  Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–1871

    Article  PubMed  CAS  Google Scholar 

  • Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174:430–440

    Article  PubMed  CAS  Google Scholar 

  • Iwański M, Rudawska M (2007) Ectomycorrhizal colonization of naturally regenerating Pinus sylvestris L. seedlings growing in different micro-habitats in boreal forest. Mycorrhiza 17:461–467

    Article  PubMed  Google Scholar 

  • Iwański M, Rudawska M, Leski T (2006) Mycorrhizal associations of nursery grown Scots pine (Pinus sylvestris L.) seedlings in Poland. Ann For Sci 63:715–723

    Article  Google Scholar 

  • Jairus T, Mpumba R, Chinoya S, Tedersoo L (2011) Invasion potential and host shifts of Australian and African ectomycorrhizal fungi in mixed eucalypt plantations. New Phytol 192:179–187

    Article  PubMed  Google Scholar 

  • Jonsson L, Dahlberg A, Nilsson M, Kårén O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal forests of Pinus sylvestris: comparative analysis of diversity of mycobionts of seedlings and old trees. New Phytol 142:151–162

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Kohout P, Sýkorová Z, Bahram M, Hadincová V, Albrechtová J, Tedersoo L, Vohník M (2011) Ericaceous dwarf shrubs affect ectomycorrhizal fungal community of the invasive Pinus strobus and native Pinus sylvestris in a pot experiment. Mycorrhiza 21:403–412

    Article  PubMed  Google Scholar 

  • Lilleskov EA, Bruns TD, Horton TR, Taylor D, Grogan P (2004) Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities. FEMS Microbiol Ecol 49:319–332

    Article  PubMed  CAS  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton Univ Pr, Princeton

    Google Scholar 

  • Menkis A, Vasaitis R (2011) Fungi in roots of nursery grown Pinus sylvestris: ectomycorrhizal colonisation, genetic diversity and spatial distribution. Microb Ecol 61:52–63

    Article  PubMed  Google Scholar 

  • Mikola P (1969) Mycorrhizal fungi of exotic forest plantations. Karstenia 10:169–175

    Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning. Chapman and Hall, New York, pp 357–423

    Google Scholar 

  • Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359

    Article  PubMed  Google Scholar 

  • O’Hanlon R, Harrington TJ (2011) Similar taxonomic richness but different communities of ectomycorrhizas in native forests and non-native plantation forests. Mycorrhiza. doi:10.1007/s00572-011-0412-0

  • O’Hanlon R, Harrington TJ (2012) Macrofungal diversity and ecology in four Irish forest types. Fungal Ecol. doi:10.1016/j.funeco.2011.12.008

  • Parker MA (2001) Mutualism as a constraint on invasion success for legumes and rhizobia. Divers Distrib 7:125–136

    Article  Google Scholar 

  • Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287

    Article  PubMed  Google Scholar 

  • Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480

    Article  PubMed  Google Scholar 

  • Peay KG, Garbelotto M, Bruns T (2010) Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology 91:3631–3640

    Article  PubMed  Google Scholar 

  • Pickles BJ, Genney DR, Potts JM, Lennon JJ, Anderson IC, Alexander IJ (2010) Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytol 186:755–768

    Article  PubMed  CAS  Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715

    Article  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, URL http: //www.R-project.org

    Google Scholar 

  • Read DJ (1998) The mycorrhizal status of Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 324–340

    Google Scholar 

  • Richardson DM (1998) Forestry trees as invasive aliens. Conserv Biol 12:18–26

    Article  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Rusca T, Kennedy P, Bruns T (2006) The effect of different pine hosts on the sampling of Rhizopogon spore banks in five Eastern Sierra Nevada forests. New Phytol 170:551–560

    Article  PubMed  CAS  Google Scholar 

  • Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140

    Article  PubMed  Google Scholar 

  • Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354

    Google Scholar 

  • Tedersoo L, Suvi T, Larsson E, Kõljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748

    Article  PubMed  Google Scholar 

  • Tedersoo L, Suvi T, Beaver K, Kõljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol 175:321–333

    Article  PubMed  CAS  Google Scholar 

  • Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Koljalg U (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490

    Article  PubMed  CAS  Google Scholar 

  • Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263

    Google Scholar 

  • Tedersoo L, Bahram M, Jairus T, Bechem E, Chinoya S, Mpumba R, Leal M, Randrianjohany E, Razafimandimbison S, Sadam A, Naadel T, Kõljalg U (2011) Spatial structure and the effects of host and soil environments on communities of ectomycorrhizal fungi in wooded savannas and rain forests of Continental Africa and Madagascar. Mol Ecol 20:3071–3080

    Article  PubMed  Google Scholar 

  • Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–884

    Article  PubMed  CAS  Google Scholar 

  • Trocha LK, Kałucka I, Stasińska M, Nowak W, Dabert M, Leski T, Rudawska M, Oleksyn J (2012) Ectomycorrhizal fungal communities of native and non-native Pinus and Quercus species in a common garden of 35-year-old trees. Mycorrhiza 22:121–134

    Article  PubMed  Google Scholar 

  • Van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  • Vellinga EC, Wolfe BE, Pringle A (2009) Global patterns of ectomycorrhizal introductions. New Phytol 181:960–973

    Article  PubMed  Google Scholar 

  • Walbert K, Ramsfield TD, Ridgway HJ, Jones EE (2010) Ectomycorrhizal species associated with Pinus radiata in New Zealand including novel associations determined by molecular analysis. Mycorrhiza 20:209–215

    Article  PubMed  CAS  Google Scholar 

  • Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton Univ Pr, Princeton

    Google Scholar 

  • Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332:1273–1277

    Article  PubMed  CAS  Google Scholar 

  • Wolfe BE, Pringle A (2012) Geographically structured host specificity is caused by the range expansions and host shifts of a symbiotic fungus. ISME J 6:745–755

    Article  PubMed  CAS  Google Scholar 

  • Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487

    Article  Google Scholar 

  • Zhang F, Hui G, Terblanche JS (2011) An interaction switch predicts the nested architecture of mutualistic networks. Ecol Lett 14:797–803

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Amin Fatahi, Hamed Shoubi, Javad Vanaei and Farhad Maleki for their help during field trips to Iran; Margit Nõukas for assisting in the laboratory; and Vilmar Veldre, Sergei Põlme, Steven Wright and Kessy Abarenkov for useful discussions. We would also like to thank Randy Molina (the editor) and two anonymous reviewers for their constructive suggestions and comments on the manuscript. We are grateful to Baba Khanjani Shiraz, Mehdi Kala Daliri, Khosro Sagheb-Talebi and the Office of Forest and Rangelands in Sari (Iran) for providing information on the plantations. This study was funded by the ESF grants 7434, 8235, RVO 67985939, Doctoral Studies and Internationalization Programme DoRa and FIBIR.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Bahram.

Supplementary material

Below is the link to the electronic supplementary material.

Table S1

List of ectomycorrhizal fungal species in ecotone, native vegetation and exotic plantations (1, presence; 0, absence) (DOC 256 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bahram, M., Kõljalg, U., Kohout, P. et al. Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa. Mycorrhiza 23, 11–19 (2013). https://doi.org/10.1007/s00572-012-0445-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-012-0445-z

Keywords

Navigation