Skip to main content
Log in

Are Trechisporales ectomycorrhizal or non-mycorrhizal root endophytes?

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Trechispora (Hydnodontaceae) is considered as a soil-inhabiting fungus. However, some species in the genus are frequently forming basidiomes on soil, a typical feature of ectomycorrhizal fungi. Ectomycorrhizal basidiomes are found in neotropical and subtropical region, but taxonomical information and DNA sequences of root fungi and basidiomes from native Atlantic Rainforest are poorly reported. Basidiomes and soil samples including roots, humus layer, and mineral soil were collected in the Atlantic Rainforest, in Florianópolis (South of Brazil). Sequences of the ITS region were obtained from all sample types and subjected to phylogenetic reconstruction. Two sequences amplified from apparently ectomycorrhizal roots belonged to Trechispora and suggested a root-associated ecology, at least biotrophic and possibly ectomycorrhizal. The analysis of isotope abundance in the same Brazilian site and in French Guiana showed that Trechispora thelephora has high 15N abundance and is often intermediate between ectomycorrhizal and saprotrophic species in 13C abundance. This is congruent with a plant biotrophic ecology, perhaps ectomycorrhizal. Future investigations in subtropical regions are needed to determine whether such a mode of nutrition is widespread among Trechispora.

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
Fig. 3

Similar content being viewed by others

References

  • Agerer R (ed) (1997) Colour Atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger GmbH, Schwäbisch-Gmünd, Germany

  • Agerer R, Christian J, Mayr C, Hobbie E (2012) Isotopic signatures and trophic status of Ramaria. Mycol Prog 11(2):47–59

    Article  Google Scholar 

  • Albee-Scott S, Kropp BR (2010) A phylogenetic study of Trechispora thelephora. Mycotaxon 114:395–399

    Article  Google Scholar 

  • Alexander I, Selosse MA (2009) Mycorrhizas in tropical forests: a neglected research imperative. New Phytol 182:14–16

    Article  PubMed  Google Scholar 

  • Alvarez-Manjarrez J, Villegas-Ríos M, Garibay-Orijel R, Contreras-Pacheco M, Kõljalg U (2016) Tomentella brunneoincrustata, the first described species of the Pisonieae-associated Neotropical Tomentella clade, and phylogenetic analysis of the genus in Mexico. Mycol Prog 15(1):1–11

    Article  Google Scholar 

  • Alvarez-Manjarrez J, Garibay-Orijel R, Smith ME (2018) Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest. Mycorrhiza 28(2):103–115

    Article  PubMed  Google Scholar 

  • Andrade ACS, Queiroz MH, Hermes RAL, Oliveira VL (2000) Mycorrhizal status of some plants of the Araucaria forest and the Atlantic rainforest in Santa Catarina, Brazil. Mycorrhiza 10(3):131–136

    Article  Google Scholar 

  • Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115

    Article  PubMed  Google Scholar 

  • Brundrett M, Tedersoo L (2019) Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol 221:18–24

    Article  PubMed  Google Scholar 

  • Corrales A, Henkel TW, Smith ME (2018) Ectomycorrhizal associations in the tropics–biogeography, diversity patterns and ecosystem roles. New Phytol 220(4):1076–1091

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid isolation procedure for small quantities of fresh tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Dunham SM, Larsson KH, Spatafora JW (2007) Species richness and community composition of mat-forming ectomycorrhizal fungi in old-and second growth Douglas-fir forests of the HJ Andrews experimental Forest, Oregon, USA. Mycorrhiza 17(8):633–645

    Article  PubMed  Google Scholar 

  • Falkenberg DB (1999) Aspectos da flora e da vegetação secundária da restinga de Santa Catarina, sul do Brasil. INSULA Rev Bot 28:01

    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(2):113–118

    Article  CAS  PubMed  Google Scholar 

  • Giachini AJ, Oliveira VL, Castellano MA, Trappe JM (2000) Ectomycorrhizal fungi in Eucalyptus and Pinus plantations in southern Brazil. Mycologia 92(6):1166–1177

    Article  Google Scholar 

  • Giachini AJ, Souza LA, Oliveira VL (2004) Species richness and seasonal abundance of ectomycorrhizal fungi in plantations of Eucalyptus dunnii and Pinus taeda in southern Brazil. Mycorrhiza 14(6):375–381

    Article  PubMed  Google Scholar 

  • Góes-Neto A, Loguercio-Leite C, Guerrero R (2005) DNA extraction from frozen field-collected and dehydrated herbarium fungal basidiomata: performance of SDS and CTAB-based methods. Biotemas 18(2):19–32

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • Halbwachs H, Easton GL, Bol R, Hobbie EA, Garnett MH, Peršoh D, Dixon L, Ostle N, Karasch P, Griffith GW (2018) Isotopic evidence of biotrophy and unusual nitrogen nutrition in soil-dwelling Hygrophoraceae. Environ Microbiol 20(10):3573–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halling RE (2001) Ectomycorrhizae: co-evolution, significance, and biogeography. Ann Mo Bot Gard 5:13

    Google Scholar 

  • Haug I, Weiß M, Homeier J, Oberwinkler F, Kottke I (2005) Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador. New Phytol 165(3):923–936

    Article  CAS  PubMed  Google Scholar 

  • Hayward J, Hynson NA (2014) New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis (Nyctaginaceae). Fungal Ecol 12:62–69

    Article  Google Scholar 

  • Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423

    Article  CAS  PubMed  Google Scholar 

  • Henkel TW, Aime MC, Chin MM, Miller SL, Vilgalys R, Smith ME (2012) Ectomycorrhizal fungal sporocarp diversity and discovery of new taxa in Dicymbe monodominant forests of the Guiana Shield. Biodivers Conserv 21(9):2195–2220

    Article  Google Scholar 

  • Henry C, Raivoarisoa JF, Razafimamonjy A, Ramanankierana H, Andrianaivomahefa P, Ducousso M, Selosse MA (2017) Transfer to forest nurseries significantly affects mycorrhizal community composition of Asteropeia mcphersonii wildings. Mycorrhiza 27(4):321–330

    Article  PubMed  Google Scholar 

  • Hibbett DS, Bauer R, Binder M, Giachini AJ, Hosaka K, Justo A, Larsson E, Larsson KH, Lawrey JD, Miettinen O, Nagy LG, Nilsson RH, Weiss M, Thorn RG (2014) 14 Agaricomycetes. In: Systematics and evolution. Springer, Berlin, pp 373–429

    Chapter  Google Scholar 

  • Hobbie EA, Sánchez FS, Rygiewicz PT (2012) Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi. Soil Biol Biochem 48:60–68

  • Hosaka K, Bates ST, Beever RE, Castellano MA, Colgan W 3rd, Domínguez LS, Nouhra ER, Geml J, Giachini AJ, Kenney SR, Simpson NB, Spatafora JW, Trappe JM (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98(6):949–959

    Article  CAS  PubMed  Google Scholar 

  • Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2014) A novel plant–fungus symbiosis benefits the host without forming mycorrhizal structures. New Phytol 201(4):1413–1422

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Thierer T (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirk PM, Cannon PF, David JC, Stalpers JA (eds) (2008) Ainsworth and Bisby’s dictionary of the Fungi, 10th edn. Wallingford, CABI Publishing

    Google Scholar 

  • Largent DL, Johnson D, Watling R (1977) How to identify mushrooms to genus III: microscopic features. Mad River Press Inc., California

    Google Scholar 

  • Larsson KH (1994) Poroid species in Trechispora and the use of calcium oxalate crystals for species identification. Mycol Res 98(10):1153–1172

    Article  Google Scholar 

  • Larsson KH (1996) New species and combinations in Trechispora (Corticiaceae, Basidiomycotina). Nord J Bot 16(1):83–98

    Article  Google Scholar 

  • Liberta AE (1973) The genus Trechispora (Basidiomycetes, Corticiaceae). Can J Bot 51(10):1871–1892

    Article  Google Scholar 

  • Mayor JR, Schuur EA, Henkel TW (2009) Elucidating the nutritional dynamics of fungi using stable isotopes. Ecol Lett 12(2):171–183

    Article  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). San Diego Supercomput. Center, New Orleans, LA. CA pp 1–8

  • Moyersoen B (2006) Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol 172(4):753–762

    Article  PubMed  Google Scholar 

  • Mueller GM, Bills GF, Foster MS (2004) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic Press

  • Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rosenthal LM, Larsson KH, Branco S, Chung JA, Glassman SI, Liao HL, Peay KG, Smith DP, Talbot JM, Taylor JW, Vellinga EC, Vilgalys R, Bruns TD (2017) Survey of corticioid fungi in North American pinaceous forests reveals hyperdiversity, underpopulated sequence databases, and species that are potentially ectomycorrhizal. Mycologia 109(1):115–127

    Article  CAS  PubMed  Google Scholar 

  • Roy M, Schimann H, Braga-Neto R, Da Silva RA, Duque J, Frame D, Wartchow F, Neves MA (2016) Diversity and distribution of ectomycorrhizal fungi from Amazonian lowland white-sand forests in Brazil and French Guiana. Biotropica 48(1):90–100

    Article  Google Scholar 

  • Roy M, Vasco-Palacios A, Geml J, Buyck B, Delgat L, Giachini A, Grebenc T, Harrower E, Kuhar F, Magnago A, Rinaldi AC, Schimann H, Selosse M-A, Sulzbacher MA, Wartchow F, Neves M-A (2017) The (re)discovery of ectomycorrhizal symbioses in Neotropical ecosystems sketched in Florianópolis. New Phytol 214:920–923

    Article  PubMed  Google Scholar 

  • Schimann H, Roy M, Jaouen G (2019). Fungi of French Guiana. Version 1.3. Unité Mixte de Recherche EcoFoG (Ecologie des Forêts de Guyane). Occurrence dataset https://doi.org/10.15468/ymvlrp. Accessed via GBIF.org on 22 July 2019

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Miller AN (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109(16):6241–6246

    Article  PubMed  PubMed Central  Google Scholar 

  • Selosse MA, Martos F (2014) Do chlorophyllous orchids heterotrophically use mycorrhizal fungal carbon? Trends Plant Sci 19(11):683–685

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21(11):621–628

    Article  PubMed  Google Scholar 

  • Selosse MA, Dubois MP, Alvarez N (2009) Do Sebacinales commonly associate with plant roots as endophytes? Mycol Res 113(10):1062–1069

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Schneider-Maunoury L, Martos F (2018) Time to re-think fungal ecology? New Phytol 217(3):968–972

    Article  PubMed  Google Scholar 

  • Singer R, Araujo IDJDS (1979) Litter decomposition and ectomycorrhiza in Amazonian forests. 1. A comparison of litter decomposing and ectomycorrhizal basidiomycetes in latosol-terra-firme rain forest and white podzol campinarana. Acta Amazon 9(1):25–42

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) In: 3rd (ed) Mycorrhizal symbiosis. Academic Press, New York

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Sulzbacher MA, Grebenc T, García MÁ, Silva BD, Silveira A, Antoniolli ZI, Marinho P, Münzenberger B, Telleria MT, Baseia IG, Martín MP (2016) Molecular and morphological analyses confirm Rhizopogon verii as a widely distributed ectomycorrhizal false truffle in Europe, and its presence in South America. Mycorrhiza 26:377–388

    Article  PubMed  PubMed Central  Google Scholar 

  • Sulzbacher MA, Grebenc T, Giachini AJ, Baseia IG (2017) Sclerotium-forming fungi from soils of the Atlantic rainforest of northeastern Brazil. Plant Ecol Evolut 150(3):358–362

    Article  Google Scholar 

  • Suvi T, Tedersoo L, Abarenkov K, Beaver K, Gerlach J, Koljalg U (2010) Mycorrhizal symbionts of Pisonia grandis and P. sechellarum in Seychelles: identification of mycorrhizal fungi and description of new Tomentella species. Mycologia 102(3):522–533

    Article  PubMed  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(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99

    Article  Google Scholar 

  • Tedersoo L, May TW, Smith ME (2010a) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263

    Article  PubMed  Google Scholar 

  • Tedersoo L, Sadam A, Zambrano M, Valencia R, Bahram M (2010b) Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot. ISME J 4(4):465–471

    Article  PubMed  Google Scholar 

  • Tello SA, Silva-Flores P, Agerer R, Halbwachs H, Beck A, Peršoh D (2014) Hygrocybe virginea is a systemic endophyte of Plantago lanceolata. Mycol Prog 13(3):471–475

    Article  Google Scholar 

  • Vohnik M, Sadowsky JJ, Kohout P, Lhotáková Z, Nestby R, Kolařík M (2012) Novel root-fungus symbiosis in Ericaceae: sheathed ericoid mycorrhiza formed by a hitherto undescribed basidiomycete with affinities to Trechisporales. PLoS One 7(6):e39524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In  Innis MA, Gelfand DH, Sninsky JJ, and White TJ (Eds) PCR protocols: A guide to methods and applications, Academic Press, San Diego, CA, pp 315–322

  • Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276

  • Yokomizo NKS (1986) Micorrizas em essenciais florestas. Anais da I reunião brasileira sobre micorrizas. Lavras, Brasil, UFLA, p 112

    Google Scholar 

  • Zeller B, Brechet C, Maurice J-P, Le Tacon F (2007) 13C and 15N isotopic fractionation in trees, soils and fungi in a natural forest stand and a Norway spruce plantation. Ann For Sci 64:419–429

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The first author thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the master’s scholarship. We thank Lina Ribeiro Venturieri and Cony Decock for help on collecting field trips, Professor Mayara Caddah for help in Guapira opposita field identification, and one anonymous reviewer for insightful comments on an earlier version of this paper. Isotopic analyses were made at SSMIM (MNHN Paris) with technical assistance of Denis Fiorillo (UMR 7209 CNRS).

Funding

The sampling in French Guiana was funded by Nouragues field station projects and by Labex grants CEBA (ANR 10-LABX-0025) and TULIP (ANR 10-LABX-0041).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Luz Vanegas-León.

Additional information

Section Editor: Marc Stadler

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 80 kb)

ESM 2

(PDF 78 kb)

ESM 3

(PDF 192 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vanegas-León, M.L., Sulzbacher, M.A., Rinaldi, A.C. et al. Are Trechisporales ectomycorrhizal or non-mycorrhizal root endophytes?. Mycol Progress 18, 1231–1240 (2019). https://doi.org/10.1007/s11557-019-01519-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-019-01519-w

Keywords

Navigation