Skip to main content
SpringerLink
Log in

Morphology and phylogeny of four Endogone species and Sphaerocreas pubescens collected in Japan

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

Abstract

The order Endogonales within Mucoromycotina includes several ectomycorrhizal species and endophytes of lower land plants. As such, this order is a key taxon for investigation of the evolutionary process of plant–fungal symbioses. However, no taxonomic study of Endogonales based on morphological and phylogenetic data has been performed, and the geographic distribution of this order in Asia remains largely unknown. We collected E. incrassata, E. pisiformis, E. flammicorona, and E. lactiflua from forests in Japan, thus representing their first description in Asia. Collected sporocarps were examined microscopically to observe details of hyphal structures, particularly in zygosporangia and gametangia. In addition, we collected Japanese Sphaerocreas pubescens, recently reported to be related to Endogone-like mycobionts of liverworts, and described its morphology. Species were also analyzed phylogenetically based on large-subunit nuclear ribosomal RNA gene sequences. The phylogenetic relationships of the four Endogone species were supported by their zygosporangial morphogenesis: group A, comprising E. incrassata and E. pisiformis, formed homogametic zygosporangia with pale-colored sporangiothecia, whereas species in group B, E. flammicorona and E. lactiflua, formed heterogametic zygosporangia with orange-colored sporangiothecia. Sphaerocreas pubescens was phylogenetically close to Densospora solicarpa, which is an uncertain zygomycotan ectomycorrhizal fungus; however, the relationship between the “Sphaerocreas/Densospora” clade and Endogone was unclear.

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

Similar content being viewed by others

References

  • Atkinson GF (1918) The genus Endogone. Brooklyn Bot Gard Mem 1:1–17

    Google Scholar 

  • Barroetaveña C, Rajchenberg M (2003) Mycorrhizas and Pseudotsuga menziesii (Mirb.) Franco seedlings production in Patagonia, Argentina. Bosque 24:3–15

    Google Scholar 

  • Berch SM, Fortin JA (1983) Germination of zygospores of Endogone pisiformis. Mycologia 75:328–332

    Article  Google Scholar 

  • Berch SM, Fortin JA (1984) Some sporocarpic Endogonaceae from eastern Canada. Can J Bot 62:170–180

    Article  Google Scholar 

  • Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577

    Article  PubMed Central  PubMed  Google Scholar 

  • Bucholtz F (1901) Hypogaeen aus Russland. Hedwigia 40:304–322

    Google Scholar 

  • Bucholtz F (1912) Beiträge zur Kenntnis der Gattung Endogone Link. Beih Bot Zent 39:147–224

    Google Scholar 

  • Calonge FD, Pasabán PM (1993) Nuevos datos sobre los hongos hipogeos de España. V. Registro de nueve citas nuevas. Bol Soc Micol Madr 18:41–57

    Google Scholar 

  • Chu-Chou M, Grace LJ (1979) Endogone flammicorona as a mycorrhizal symbiont of Douglas fir in New Zealand. N Z J For Sci 9:344–347

    Google Scholar 

  • Chu-Chou M, Grace LJ (1984) Endogone flammicorona and Tuber sp. as mycorrhizal fungi of Pinus radiata in New Zealand. N Z J Bot 22:525–531

    Article  Google Scholar 

  • Chu-Chou M, Grace LJ (1988) Mycorrhizal fungi of radiata pine in different forests of the North and South islands in New Zealand. Soil Biol Biochem 20:883–886

    Article  Google Scholar 

  • Clémençon H (2009) Methods for Working with Macrofungi: Laboratory Cultivation and Preparation of Larger Fungi for Light Microscopy. IHW-Verlag, Eching

    Google Scholar 

  • Degawa Y, Gams W (2004) A new species of Mortierella, and an associated sporangiiferous mycoparasite in a new genus, Nothadelphia. Stud Mycol 50:567–572

    Google Scholar 

  • Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: a chequered history. Proc Biol Sci. doi:10.1098/rspb.2013.0207

    PubMed Central  PubMed  Google Scholar 

  • Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P (2015) Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol 205:1464–1472

    Article  PubMed  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 

  • Fassi B (1965) Micorrize ectotrofiche di « Pinus strobus » L. prodotte da un'Endogone (« Endogone lactiflua» Berk.). Allionia 11:7–15

    Google Scholar 

  • Fassi B, Palenzona M (1969) Sintesi micorrizica tra «Pinus strobus», «Pseudotsuga douglasii» ed «Endogone lactiflua». Allionia 15:105–114

    Google Scholar 

  • Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2015) First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytol 205:743–756

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fischer E (1897) Tuberineae und Plectascineae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzfamilien I. Verlag von Wilhelm Engelmann, Leipzig, pp 278–320

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gäumann EA, Dodge CW (1928) Comparative morphology of fungi. McGraw-Hill, New York

    Google Scholar 

  • Gerdemann JW, Trappe JM (1970) Endogone incrassata: a zygosporic species with hollow sporocarps. Mycologia 62:1204–1208

    Article  Google Scholar 

  • Gerdemann JW, Trappe JM (1974) Endogonaceae in the Pacific Northwest. Mycol Mem 5:1–76

    Google Scholar 

  • Gibson JL, Kimbrough JW, Benny GL (1986) Ultrastructural observations on Endogonaceae (Zygomycetes). II. Glaziellales ord. nov. and Glaziellaceae fam. nov.: new taxa based upon light and electron microscopic observations of Glaziella aurantiaca. Mycologia 78:941–954

    Article  Google Scholar 

  • Godfrey RM (1957) Studies of British species of Endogone. I. Morphology and taxonomy. Trans Br Mycol Soc 40:117–135

    Article  Google Scholar 

  • Gourley CO (1982) An annotated index of the fungi of Nova Scotia. Proc N S Inst Sci 32:75–293

    Google Scholar 

  • Hall IR (1977) Species and mycorrhizal infections of New Zealand Endogonaceae. Trans Br Mycol Soc 68:341–356

    Article  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüssler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • Hirose D, Degawa Y, Inaba S, Tokumasu S (2012) The anamorphic genus Calcarisporiella is a new member of the Mucoromycotina. Mycoscience 53:256–260

    Article  Google Scholar 

  • Hirose D, Degawa Y, Yamamoto K, Yamada A (2014) Sphaerocreas pubescens is a member of the Mucoromycotina closely related to fungi associated with liverworts and hornworts. Mycoscience 55:221–226

    Article  CAS  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüssler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Yu H, Xiang M, Liu X, Liu X (2011) Echinochlamydosporium variabile, a new genus and species of Zygomycota from soil nematodes. Fungal Divers 46:43–51

    Article  Google Scholar 

  • Kanouse BB (1936) Studies of two species of Endogone in culture. Mycologia 28:47–62

    Article  Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:276–285

    Article  Google Scholar 

  • Koske RE, Gemma JN, Olexia PD (1986) Glomus microaggregatum, a new species in the Endogonaceae. Mycotaxon 26:125–132

    Google Scholar 

  • Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223

    Article  PubMed  Google Scholar 

  • Lihnell D (1937) Fynd av Endogone pisiformis Link och Tuber maculatum Vitt. vid Uppsala. Sven bot tidskr 31:150

    Google Scholar 

  • Link HF (1809) Observationes in ordines plantarum naturales. Dissertatio I. Mag Ges Naturf Freunde Berl 3:3–42

    Google Scholar 

  • May T (1997) Fungi from the mycology post-conference foray October 1996. Australas Mycol Newsl 16:35–37

    Google Scholar 

  • McGee PA (1986) Further sporocarpic species of Glomus (Endogonaceae) from south Australia. Trans Br Mycol Soc 87:123–129

    Article  Google Scholar 

  • McGee PA (1996) The Australian zygomycetous mycorrhizal fungi: the genus Densospora gen. nov. Aust Syst Bot 9:329–336

    Article  Google Scholar 

  • McGee PA, Trappe JM (2002) The Australian zygomycetous mycorrhizal fungi. II. Further Australian sporocarpic Glomaceae. Aust Syst Bot 15:115–124

    Article  Google Scholar 

  • Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes) a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471–491

    Google Scholar 

  • Nicolson TH, Gerdemann JW (1968) Mycorrhizal Endogone species. Mycologia 60:313–325

    Article  Google Scholar 

  • O’Donnell K, Lutzoni FM, Ward TJ, Benny GL (2001) Evolutionary relationships among mucoralean fungi (Zygomycota): evidence for family polyphyly on a large scale. Mycologia 93:286–297

    Article  Google Scholar 

  • Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G, Mizzan L, Garbelotto MM (2013) Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PLoS One 8:e62419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pap G, Pazmany D, Misky M (1990) New data regarding hypogeous mushrooms of Romania (III). Not Bot Hort Agrobot Cluj 20:17–21

    Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 10:763–765

    Article  Google Scholar 

  • Paz I, Barrio L, Lavoise C (2013) Catálogo provisional de hongos hipogeos de Cantabria y posibles fitobiontes asociados. Yesca 25:137–166

    Google Scholar 

  • Pegler DN, Spooner BM, Young TWK (1993) British truffles. Royal Botanic Gardens, Kew, Surrey, England

    Google Scholar 

  • Petch T (1925) Additions to Ceylon fungi, III. Ann R Bot Gard Perad 9:313–328

    Google Scholar 

  • Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book? New Phytol 205:1394–1398

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed Central  PubMed  Google Scholar 

  • Saccardo PA (1882) Fungi boreali-Americani. Michelia 2:564–582

    Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tandy PA (1975a) Sporocarpic species of Endogonaceae in Australia. Aust J Bot 23:849–866

    Article  Google Scholar 

  • Tandy PA (1975b) Studies of sporocarpic Endogonaceae in Australia. University of Adelaide, Dissertation

    Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Tedersoo L (2007) Ectomycorrhizal fungi: diversity and community structure in Estonia, Seychelles and Australia. University of Tartu, Dissertation

    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 

  • Thaxter R (1922) A revision of the Endogoneae. Proc Am Acad Arts Sci 57:291–351

    Article  Google Scholar 

  • Trappe JM, Gerdemann JW (1972) Endogone flammicorona sp. nov. a distinctive segregate from Endogone lactiflua. Trans Br Mycol Soc 59:403–407

    Article  Google Scholar 

  • Trappe JM, Gerdemann JW (1979) A neotype of Endogone pisiformis. Mycologia 71:206–209

    Article  Google Scholar 

  • Trappe JM, Schenck NC (1982) Vesicular-arbuscular mycorrhizal fungi (Endogonales). In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, Minnesota, pp 1–9

    Google Scholar 

  • Vidal JM, Vila J (1994) Algunos hongos hipogeos de Andorra. Bull Soc Catalana Micol 16–17:213–220

    Google Scholar 

  • Wagner L, Stielow B, Hoffmann K, Petkovits T, Papp T, Vágvölgyi C, de Hoog GS, Verkley G, Voigt K (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia 30:77–93

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Walker C (1985) Endogone lactiflua forming ectomycorrhizas with Pinus contorta. Trans Br Mycol Soc 84:353–355

    Article  Google Scholar 

  • Walther G, Pawłowska J, Alastruey-Izquierdo A, Wrzosek M, Rodriguez-Tudela JL, Dolatabadi S, Chakrabarti A, de Hoog GS (2013) DNA barcoding in Mucorales: an inventory of biodiversity. Persoonia 30:11–47

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warcup JH (1985) Ectomycorrhizal formation by Glomus tubiforme. New Phytol 99:267–272

    Article  Google Scholar 

  • Warcup JH (1990) Taxonomy, culture and mycorrhizal associations of some zygosporic Endogonaceae. Mycol Res 94:173–178

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal 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 

  • Wu CG, Lin SJ (1997) Endogonales in Taiwan: a new genus with unizygosporic sporocarps and a hyphal mantle. Mycotaxon 64:179–188

    Google Scholar 

  • Yao YJ, Pegler DN, Young TWK (1992) Revision of the type of Endogone alba (Endogonaceae). Mycotaxon 45:109–122

    Google Scholar 

  • Yao YJ, Pegler DN, Young TWK (1995) Youngiomyces, a new genus in Endogonales (Zygomycotina). Kew Bull 50:349–357

    Article  Google Scholar 

  • Yao YJ, Pegler DN, Young TWK (1996) Genera of Endogonales. Royal Botanic Gardens, Kew, Surrey, England

    Google Scholar 

Download references

Acknowledgments

We are grateful to the members of the Mycorrhiza Laboratory, Shinshu University, and the Laboratory of Mycology, Sugadaira, and Mr. Yusuke Takashima for donation of the specimens and support for our sampling. Mr. Tetsuo Muroi kindly provided valuable literature regarding Endogonales. We also thank Dr. Kentaro Hosaka (TNS), Mr. Daisuke Sakuma (OSA), and Dr. Takamichi Orihara (KPM), who allowed access to the herbarium specimens and deposits of our specimens. In addition, we thank the technical staff of the Division of Instrumental Analysis, Research Center for Human and Environmental Sciences, Shinshu University, for DNA sequencing. This study was supported in part by a Research Fellowship for Young Scientists (No. 14J09199) from the Japan Society for the Promotion of Science (JSPS).

Author information

Authors and Affiliations

  1. Department of Bioscience and Food Production Science, Interdisciplinary Graduate School of Science and Technology, Shinshu University, Minami-minowa, Nagano, 399-4598, Japan

    Kohei Yamamoto & Akiyoshi Yamada

  2. Sugadaira Montane Research Center, University of Tsukuba, Sugadaira Kogen, Nagano, 386-2204, Japan

    Yousuke Degawa

  3. College of Pharmacy, Nihon University, Funabashi, Chiba, 274-8555, Japan

    Dai Hirose

  4. Department of Bioscience and Biotechnology, Faculty of Agriculture, Shinshu University, Minami-minowa, Nagano, 399-4598, Japan

    Masaki Fukuda & Akiyoshi Yamada

  5. Division of Terrestrial Ecosystem, Institute of Mountain Science, Shinshu University, Minami-minowa, Nagano, 399-4598, Japan

    Akiyoshi Yamada

Authors
  1. Kohei Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yousuke Degawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dai Hirose
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masaki Fukuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akiyoshi Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kohei Yamamoto.

Additional information

Section Editor: Franz Oberwinkler

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamamoto, K., Degawa, Y., Hirose, D. et al. Morphology and phylogeny of four Endogone species and Sphaerocreas pubescens collected in Japan. Mycol Progress 14, 86 (2015). https://doi.org/10.1007/s11557-015-1111-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-015-1111-6

Keywords

Search

Navigation