Mycological Progress

, Volume 18, Issue 9, pp 1231–1240 | Cite as

Are Trechisporales ectomycorrhizal or non-mycorrhizal root endophytes?

  • Mary Luz Vanegas-LeónEmail author
  • Marcelo A. Sulzbacher
  • Andrea C. Rinaldi
  • Mélanie Roy
  • Marc-André Selosse
  • Maria Alice Neves
Original Article


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.


Atlantic rainforest Biotrophic nutrition Ectomycorrhizal fungi Isotopic analysis ITS Phylogenetic analysis 



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 information

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).

Supplementary material

11557_2019_1519_MOESM1_ESM.pdf (81 kb)
ESM 1 (PDF 80 kb)
11557_2019_1519_MOESM2_ESM.pdf (79 kb)
ESM 2 (PDF 78 kb)
11557_2019_1519_MOESM3_ESM.pdf (192 kb)
ESM 3 (PDF 192 kb)


  1. Agerer R (ed) (1997) Colour Atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger GmbH, Schwäbisch-Gmünd, GermanyGoogle Scholar
  2. Agerer R, Christian J, Mayr C, Hobbie E (2012) Isotopic signatures and trophic status of Ramaria. Mycol Prog 11(2):47–59CrossRefGoogle Scholar
  3. Albee-Scott S, Kropp BR (2010) A phylogenetic study of Trechispora thelephora. Mycotaxon 114:395–399CrossRefGoogle Scholar
  4. Alexander I, Selosse MA (2009) Mycorrhizas in tropical forests: a neglected research imperative. New Phytol 182:14–16CrossRefPubMedGoogle Scholar
  5. 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):1–11CrossRefGoogle Scholar
  6. 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):103–115CrossRefPubMedGoogle Scholar
  7. 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):131–136CrossRefGoogle Scholar
  8. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115CrossRefPubMedGoogle Scholar
  9. Brundrett M, Tedersoo L (2019) Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol 221:18–24CrossRefPubMedGoogle Scholar
  10. Corrales A, Henkel TW, Smith ME (2018) Ectomycorrhizal associations in the tropics–biogeography, diversity patterns and ecosystem roles. New Phytol 220(4):1076–1091CrossRefGoogle Scholar
  11. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772CrossRefPubMedPubMedCentralGoogle Scholar
  12. Doyle JJ, Doyle JL (1987) A rapid isolation procedure for small quantities of fresh tissue. Phytochem Bull 19:11–15Google Scholar
  13. 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):633–645CrossRefPubMedGoogle Scholar
  14. Falkenberg DB (1999) Aspectos da flora e da vegetação secundária da restinga de Santa Catarina, sul do Brasil. INSULA Rev Bot 28:01Google Scholar
  15. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118CrossRefGoogle Scholar
  16. Giachini AJ, Oliveira VL, Castellano MA, Trappe JM (2000) Ectomycorrhizal fungi in Eucalyptus and Pinus plantations in southern Brazil. Mycologia 92(6):1166–1177CrossRefGoogle Scholar
  17. 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):375–381CrossRefPubMedGoogle Scholar
  18. 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):19–32Google Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704CrossRefGoogle Scholar
  20. 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):3573–3588CrossRefPubMedGoogle Scholar
  21. Halling RE (2001) Ectomycorrhizae: co-evolution, significance, and biogeography. Ann Mo Bot Gard 5:13Google Scholar
  22. 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):923–936CrossRefPubMedGoogle Scholar
  23. Hayward J, Hynson NA (2014) New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis (Nyctaginaceae). Fungal Ecol 12:62–69CrossRefGoogle Scholar
  24. Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423CrossRefPubMedGoogle Scholar
  25. 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):2195–2220CrossRefGoogle Scholar
  26. 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):321–330CrossRefPubMedGoogle Scholar
  27. 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 373–429CrossRefGoogle Scholar
  28. Hobbie EA, Sánchez FS, Rygiewicz PT (2012) Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi. Soil Biol Biochem 48:60–68Google Scholar
  29. 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):949–959CrossRefPubMedGoogle Scholar
  30. 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):1413–1422CrossRefPubMedGoogle Scholar
  31. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kirk PM, Cannon PF, David JC, Stalpers JA (eds) (2008) Ainsworth and Bisby’s dictionary of the Fungi, 10th edn. Wallingford, CABI PublishingGoogle Scholar
  34. Largent DL, Johnson D, Watling R (1977) How to identify mushrooms to genus III: microscopic features. Mad River Press Inc., CaliforniaGoogle Scholar
  35. Larsson KH (1994) Poroid species in Trechispora and the use of calcium oxalate crystals for species identification. Mycol Res 98(10):1153–1172CrossRefGoogle Scholar
  36. Larsson KH (1996) New species and combinations in Trechispora (Corticiaceae, Basidiomycotina). Nord J Bot 16(1):83–98CrossRefGoogle Scholar
  37. Liberta AE (1973) The genus Trechispora (Basidiomycetes, Corticiaceae). Can J Bot 51(10):1871–1892CrossRefGoogle Scholar
  38. Mayor JR, Schuur EA, Henkel TW (2009) Elucidating the nutritional dynamics of fungi using stable isotopes. Ecol Lett 12(2):171–183CrossRefPubMedGoogle Scholar
  39. 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 1–8Google Scholar
  40. Moyersoen B (2006) Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol 172(4):753–762CrossRefPubMedGoogle Scholar
  41. Mueller GM, Bills GF, Foster MS (2004) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic PressGoogle Scholar
  42. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45Google Scholar
  43. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574CrossRefGoogle Scholar
  44. 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):115–127CrossRefPubMedGoogle Scholar
  45. 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):90–100CrossRefGoogle Scholar
  46. 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 214:920–923CrossRefPubMedGoogle Scholar
  47. 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 Accessed via on 22 July 2019
  48. 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):6241–6246CrossRefPubMedGoogle Scholar
  49. Selosse MA, Martos F (2014) Do chlorophyllous orchids heterotrophically use mycorrhizal fungal carbon? Trends Plant Sci 19(11):683–685CrossRefPubMedGoogle Scholar
  50. Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21(11):621–628CrossRefPubMedGoogle Scholar
  51. Selosse MA, Dubois MP, Alvarez N (2009) Do Sebacinales commonly associate with plant roots as endophytes? Mycol Res 113(10):1062–1069CrossRefPubMedGoogle Scholar
  52. Selosse MA, Schneider-Maunoury L, Martos F (2018) Time to re-think fungal ecology? New Phytol 217(3):968–972CrossRefPubMedGoogle Scholar
  53. 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):25–42CrossRefGoogle Scholar
  54. Smith SE, Read DJ (2008) In: 3rd (ed) Mycorrhizal symbiosis. Academic Press, New YorkGoogle Scholar
  55. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 26:377–388CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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):358–362CrossRefGoogle Scholar
  58. 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):522–533CrossRefPubMedGoogle Scholar
  59. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99CrossRefGoogle Scholar
  61. Tedersoo L, May TW, Smith ME (2010a) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263CrossRefGoogle Scholar
  62. 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):465–471CrossRefPubMedGoogle Scholar
  63. 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):471–475CrossRefGoogle Scholar
  64. 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):e39524CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363CrossRefPubMedGoogle Scholar
  66. 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 315–322Google Scholar
  67. Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276Google Scholar
  68. Yokomizo NKS (1986) Micorrizas em essenciais florestas. Anais da I reunião brasileira sobre micorrizas. Lavras, Brasil, UFLA, p 112Google Scholar
  69. 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 64:419–429CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biologia de Fungos, Algas e Plantas, Departamento de BotânicaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Departamento de solosUniversidade Federal de Santa MariaSanta MariaBrazil
  3. 3.Dipartimento di Scienze BiomedicheUniversità di CagliariMonserratoItaly
  4. 4.Laboratoire Evolution et Diversité BiologiquePaul Sabatier University - Toulouse III ToulouseFrance
  5. 5.Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum national d’Histoire naturelle, CNRSSorbonne UniversitéParisFrance
  6. 6.Department of Plant Taxonomy and Nature ConservationUniversity of GdańskGdańskPoland

Personalised recommendations