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Assessing ectomycorrhizal fungal spore banks of truffle producing soils with pecan seedling trap-plants

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Abstract

Background and Aims

Recently, the truffle species Tuber lyonii Butters was found to be dominant in ectomycorrhizal (EcM) fungal communities of cultivated pecan (Carya illinoinensis (Wangenh.) K. Koch). Many truffle fungi exhibit the trait of effectively colonizing plant roots via spores. We hypothesized that T. lyonii would be well represented in the spore bank of pecan orchard soils where it is found.

Methods

We used axenically-grown pecan seedlings as trap-plants to bait for EcM associates in soils collected beneath truffle-producing pecan trees. EcM fungi on seedlings were characterized through rDNA sequencing and were compared to EcM communities of adult trees in these orchards.

Results

Tuber lyonii mycorrhizas were well formed on seedlings inoculated with truffle spores, but were limited to just a few of the trap-plants grown in field soils. We compared EcM communities of adult pecan orchard trees to those on trap-plants and found distinct communities on each, with a high degree of similarity at the ordinal but not species level.

Conclusions

Although species of Pezizales are abundant in pecan EcM communities and as propagules in their soil spore banks, only a low level of T. lyonii was detected in soil spore banks beneath orchard trees naturally colonized by T. lyonii. Other factors including land-use history or orchard management may better explain this truffle species presence and abundance in pecan EcM communities.

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Abbreviations

EcM:

ectomycorrhizal

References

  • Agerer R (2001) Exploration types of ectomycorrhizae—a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418

    Article  Google Scholar 

  • Bidartondo MI, Baar J, Bruns TD (2001) Low ectomycorrhizal inoculum potential and diversity from soils in and near ancient forests of bristlecone pine (Pinus longaeva). Can J Bot 79:293–299

    Google Scholar 

  • Bonito G, Isikhuemhen OS, Vilgalys R (2010) Identification of fungi associated with municipal compost using DNA-based techniques. Bioresour Technol 101:1021–1027

    Article  PubMed  CAS  Google Scholar 

  • Bonito G, Brenneman T, Vilgalys R (2011a) Ectomycorrhizal fungal diversity in orchards of cultivated pecan (Carya illinoinensis; Juglandaceae). Mycorrhiza 21:601–612

    Article  PubMed  Google Scholar 

  • Bonito G, Trappe JM, Donovan S, Vilgalys R (2011b) The Asian black truffle Tuber indicum can form ectomycorrhizas with North American host plants and complete its life cycle in non-native soils. Funct Ecol 4:83–93

    Google Scholar 

  • Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP (2009) Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytol 181:463–470

    Article  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) Qiime allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed  CAS  Google Scholar 

  • Carey AB, Colgan W, Trappe JM, Molina R (2002) Effects of forest management on truffle abundance and squirrel diets. NW Sci 76:148–157

    Google Scholar 

  • Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255

    Article  Google Scholar 

  • Edgar RC (2004) Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1–19

    Article  Google Scholar 

  • Fox FM (1983) Role of basidiospores as inocula of mycorrhizal fungi of birch. Plant Soil 71:269–273

    Article  Google Scholar 

  • Frank JL, Anglin S, Carrington EM, Taylor DS, Viratos B, Southworth D (2009) Rodent dispersal of fungal spores promotes seedling establishment away from mycorrhizal networks on Quercus garryana. Botany 87:821–829

    Article  CAS  Google Scholar 

  • Fujimura KF, Smith JE, Horton TR, Weber NS, Spatafora JW (2005) Pezizalean mycorrhizas and sporocarps in ponderosa pine (Pinus ponderosa) after prescribed fires in eastern Oregon, USA. Mycorrhiza 15:79–86

    Article  PubMed  CAS  Google Scholar 

  • Gehring CA, Theimer TC, Whitham TG, Keim P (1998) Ectomycorrhizal fungal community structure of pinyon pines growing in two environmental extremes. Ecology 79:1562–1572

    Article  Google Scholar 

  • Grubisha LC, Bergemann SE, Bruns TD (2007) Host islands within the California northern channel islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon. Mol Ecol 16:1811–1822

    Article  PubMed  Google Scholar 

  • Hausmann NT, Hawkes CV (2010) Order of plant host establishment alters the composition of arbuscular mycorrhizal communities. Ecology 91:2333–2343

    Article  PubMed  Google Scholar 

  • Horton TR, Cázares E, Bruns TD (1998) Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza 8:11–18

    Article  Google Scholar 

  • Izzo AD, Meyer M, Trappe JM, North M, Bruns TD (2005) Hypogeous ectomycorrhizal fungal species on roots and in small mammal diet in a mixed-conifer forest. Forest Sci 51:243–254

    Google Scholar 

  • Johnson CN (1996) Interactions between mammals and ectomycorrhizal fungi. Trends Ecol Evol 11:503–507

    Article  PubMed  CAS  Google Scholar 

  • Jumpponen A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytol 158:569–578

    Article  Google Scholar 

  • Jumpponen A, Trappe JM, Cázares E (1999) Ectomycorrhizal fungi in Lyman lake basin: a comparison between primary and secondary successional sites. Mycologia 91:575–582

    Article  Google Scholar 

  • Kennedy PG, Bruns TD (2005) Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytol 166:631–638

    Article  PubMed  Google Scholar 

  • Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 90:2098–2107

    Article  PubMed  Google Scholar 

  • Kjoller R (2006) Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol Ecol 58:214–224

    Article  PubMed  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  CAS  Google Scholar 

  • Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97:762–769

    Article  PubMed  Google Scholar 

  • Louette G, De Meester L, Declerck S (2008) Assembly of zooplankton communities in newly created ponds. Freshwat Biol 53:2309–2320

    Google Scholar 

  • Maddison D, Maddison W (2002) Macclade: analysis of phylogeny and character evolution. Sunderland: Sinauer Associates. 4.0

  • Mamoun M, Oliver JM (1997) Mycorrhizal inoculation of cloned hazels by Tuber melanosporum: effect of soil disinfestation and co-culture with Festuca ovina. Plant Soil 188:221–226

    Article  CAS  Google Scholar 

  • Markewitz D, Richter DD, Allen HL, Urrego JB (1998) Three decades of observed soil acidification in the Calhoun experimental forest: has acid rain made a difference? Soil Sci Soc Am J 62:1428–1439

    Article  CAS  Google Scholar 

  • Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178

    Article  PubMed  CAS  Google Scholar 

  • Nara K (2009) Spores of ectomycorrhizal fungi: ecological strategies for germination and dormancy. New Phytol 181:245–248

    Article  PubMed  Google Scholar 

  • Newton AC (1992) Towards a functional classification of ectomycorrhizal fungi. Mycorrhiza 2:75–79

    Article  Google Scholar 

  • Parlade J, Pera J, Alvarez IF (1996) Inoculation of containerized Pseudotsuga menziesii and Pinus pinaster seedlings with spores of five species of ectomycorrhizal fungi. Mycorrhiza 6:237–245

    Article  Google Scholar 

  • Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Biosci 58:799–810

    Article  Google Scholar 

  • Peay KG, Garbelotto M, Bruns TD (2009) Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings. J Ecol 97:537–547

    Article  Google Scholar 

  • Robinson JV, Dickerson JE (1987) Does invasion sequence affect community structure. Ecol 68:587–595

    Article  Google Scholar 

  • Rusca TA, Kennedy PG, Bruns TD (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 

  • Simard SW, Perry DA, Smith JE, Molina R (1997) Effects of soil trenching on occurrence of ectomycorrhizas on Pseudotsuga menziesii seedlings grown in mature forests of Betula papyrifera and Pseudotsuga menziesii. New Phytol 136:327–340

    Article  Google Scholar 

  • Smith ME, Douhan GW, Rizzo DM (2007a) Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytol 174:847–863

    Article  PubMed  CAS  Google Scholar 

  • Smith ME, Douhan GW, Rizzo DM (2007b) Intra-specific and intra-sporocarp ITS variation of ectomycorrhizal fungi as assessed by rDNA sequencing of sporocarps and pooled ectomycorrhizal roots from a Quercus woodland. Mycorrhiza 18:15–22

    Article  PubMed  CAS  Google Scholar 

  • Sparks D (1976) Soil pH and the pecan. 67th Annual Report of the Northern Nut Growers Association, pp. 93-99

  • Swofford DL (2002) Paup* phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts. Sinauer Associates. 4.0

  • Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850

    Article  PubMed  CAS  Google Scholar 

  • Tedersoo L, Hansen K, Perry BA, Kjoller R (2006) Molecular and morphological diversity of pezizalean ectomycorrhiza. New Phytol 170:581–596

    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

    Article  PubMed  Google Scholar 

  • Trappe JM (1975) Generic synonyms in the Tuberales. Mycotaxon 2:109–122

    Google Scholar 

  • Urban A, Neuner-Plattner I, Krisai-Greilhuber I, Haselwandter K (2004) Molecular studies on terricolous microfungi reveal novel anamorphs of two Tuber species. Mycol Res 108:749–758

    Article  PubMed  CAS  Google Scholar 

  • Visser S (1995) Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytol 129:389–401

    Article  Google Scholar 

  • Warcup JH (1990) Occurrence of ectomycorrhizal and saprophytic discomycetes after a wild fire in a eucalypt forest. Mycol Res 94:1065–1069

    Article  Google Scholar 

  • Warcup JH (1991) The fungi forming mycorrhizas on eucalypt seedlings in regeneration coupes in Tasmania. Mycol Res 95:329–332

    Article  Google Scholar 

  • Ward SA, Thornton IWB (2000) Chance and determinism in the development of isolated communities. Glob Ecol Biogeogr 9:7–18

    Article  Google Scholar 

  • Warr SJ, Thompson K, Kent M (1993) Seed banks as a neglected area of biogeographic research—a review of literature and sampling techniques. Progr Phys Geogr 17:329–347

    Article  Google Scholar 

  • Wedén C, Pettersson L, Danell E (2009) Truffle cultivation in Sweden: results from Quercus robur and Corylus avellana field trials on the island of Gotland. Scand J Forest Res 24:37–53

    Article  Google Scholar 

  • Yun W, Hall IR (2004) Edible ectomycorrhizal mushrooms: challenges and achievements. Can J Bot 82:1063–1073

    Article  Google Scholar 

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Acknowledgements

The authors thank the willingness and cooperation of the Magnolia and Pine Knoll pecan farms for participating in this study. We thank Bernadette O’Reilley and Allen Lowrance for field assistance. Thanks to Connie Robertson for curating truffle collections for the Duke herbarium. Bill Bunn was kind to provide pecans for this study. We appreciate the constructive feedback given by two anonymous reviewers. This study was made possible through NSF funding to RV and GB (DBI-0710213). The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Biology Department, Duke University, Durham, NC, 27708, USA

    Gregory Bonito & Rytas Vilgalys

  2. Department of Plant Pathology, University of Florida, Gainesville, FL, 32611, USA

    Matthew E. Smith

  3. Department of Plant Pathology, University of Georgia, Tifton, GA, 31794, USA

    Timothy Brenneman

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  1. Gregory Bonito
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  2. Matthew E. Smith
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  4. Rytas Vilgalys
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Correspondence to Gregory Bonito.

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Responsible Editor: Thom W. Kuyper.

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Bonito, G., Smith, M.E., Brenneman, T. et al. Assessing ectomycorrhizal fungal spore banks of truffle producing soils with pecan seedling trap-plants. Plant Soil 356, 357–366 (2012). https://doi.org/10.1007/s11104-012-1127-5

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