Skip to main content
Log in

Molecular phylogenetic analyses show that Amanita ovoidea and Amanita proxima are distinct species and suggest their assignment to Roanokenses section

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

Abstract

Amanita ovoidea is generally considered edible and is morphologically similar to Amanita proxima that contains nephrotoxins. Both species were assigned to Amanita section Amidella. To study their phylogenetic relationships, we performed nrITS- and RPB2-based analyses of these and other Amanita species. Our analyses show that (i) A. ovoidea and A. proxima are distinct species; (ii) A. ovoidea has an extensively heterogeneous ITS with up to 4.4% pairwise genetic distance between individuals; (iii) in A. ovoidea, pairwise genetic distance between ITS clones from a single basidiome was as high as 3.2%, possibly because of hybridization events and subsequent failure of the rDNA repeats to homogenize; (iv) A. aminoaliphatica and A. proxima are taxonomic synonyms; and (v) A. proxima and A. ovoidea cluster with species belonging to section Roanokenses rather than with those of section Amidella sensu stricto. This study supports the development of species-specific markers for diagnosis of the toxic and the edible species here examined.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bas C (1969) Morphology and subdivision of Amanita and a monograph of its section Lepidella. Persoonia 5:285–579

    Google Scholar 

  • Bellù F (2009) Notes on fungal toxicology. Bresadoliana 1:88–94

    Google Scholar 

  • Beutler JA, der Marderosian AH (1981) Chemical variation in Amanita. J Nat Prod 44:422–431

    Article  CAS  Google Scholar 

  • Biagi M, Martelli L, Perini C, Di Lella L, Miraldi E (2014) Investigations into Amanita ovoidea (bull.) Link.: edible or poisonous? Nat Res Forum 5:225–232

    Google Scholar 

  • Cai Q, Tulloss RE, Tang LP, Tolgor B, Zhang P, Chen ZH, Yang ZL (2014) Multi-locus phylogeny of lethal amanitas: implications for species diversity and historical biogeography. BMC Evol Biol 14:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen ZH, Zhang P, Zhang ZG (2014) Investigation and analysis of 102 mushroom poisoning cases in southern China from 1994 to 2012. Fungal Divers 64:123–131

    Article  Google Scholar 

  • Courtin P, Gallardo M, Berrouba A, Drouet G, de Haro L (2009) Renal failure after ingestion of Amanita proxima. Clin Toxicol 47:906–908

    Article  Google Scholar 

  • Cui YY, Cai Q, Tang LP, Liu JW, Yang ZL (2018) The family Amanitaceae: molecular phylogeny, higher rank taxonomy and the species in China. Fungal Divers 91:5–230

    Article  Google Scholar 

  • Diaz JH (2016) Mistaken mushroom poisonings. Wild Environ Med 27:330–335

    Article  Google Scholar 

  • Drehmel D, Moncalvo JM, Vilgalys R (1999) Molecular phylogeny of Amanita based on large-subunit ribosomal DNA sequences: implications for taxonomy and character evolution. Mycologia 91:610–618

    Article  CAS  Google Scholar 

  • Dumée P (1916) Notes de mycologie pratique. 4. Note sur une amanite voisine d'Amanita ovoidea, Amanita proxima Dumée nov. sp B Soc Mycol Fr 32:83–86

  • Filippi I (1985) Una nuova Amanita dell’area mediterranea. Micol Ital 14:15–19

    Google Scholar 

  • Filippi I (1993) Attenzione ai funghi tossici. Micol Ital 3:163–164

    Google Scholar 

  • Fu XY, Fu B, He ZM, Gong MM, Li ZG, Chen ZH (2017) Acute renal failure caused by Amanita oberwinklerana poisoning. Mycoscience 58:121–127

    Article  Google Scholar 

  • Garcia J, Oliviera A, Guedes de Pinho P, Freitas V, Carvalho A, Baptista P, Pereira E, Bastos M, Carvalho F (2015) Determination of amatoxins and phallotoxins in Amanita phalloides mushrooms from northern Portugal by HPLC-DAD-MS. Mycologia 107:679–687

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gilbert EJ (1940) Amanitaceae. Iconogr Mycol (Milano) 27, suppl. (1–3): i–xx, 1–427, 73 pl.

  • Granziero A (2006) Morphobotanical aspects of Amanita ovoidea and A. proxima. Pagine di Micologia 25:25–26

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98

    CAS  Google Scholar 

  • Harpke D, Peterson A (2006) Non-concerted ITS evolution in Mammillaria (Cactaceae). Mol Phylogenet Evol 41:579–593

    Article  CAS  PubMed  Google Scholar 

  • Hughes KW, Petersen RH, Lickey EB (2009) Using heterozygosity to estimate a percentage DNA sequence similarity for environmental species’ delimitation across basidiomycete fungi. New Phytol 182:795–798

    Article  CAS  PubMed  Google Scholar 

  • Hughes KW, Petersen RH, Lodge DJ, Bergemann SE, Baumgartner K, Tulloss RE, Lickey E, Cifuentes J (2013) Evolutionary consequences of putative intra-and interspecific hybridization in agaric fungi. Mycologia 105:1577–1594

    Article  CAS  PubMed  Google Scholar 

  • Hughes KW, Tulloss RE, Petersen RH (2018) Intragenomic nuclear RNA variation in a cryptic Amanita taxon. Mycologia 110:93–103

    CAS  PubMed  Google Scholar 

  • Kirchmair M, Carrilho P, Pfab R, Haberl B, Felgueiras J, Carvalho F, Cardoso J, Melo I, Vinhas J, Neuhauser S (2012) Amanita poisonings resulting in acute, reversible renal failure: new cases, new toxic Amanita mushrooms. Nephrol Dial Transplant 27:1380–1386

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Cavoli G, Bono L, Schillaci O, Servillo F, Carollo C, Zagarrigo C, Amato A, Li Cavoli Tancredi V, Azzolina V, Caputo F (2019) Acute renal failure after Amanita ovoidea eating. Indian J Nephrol 29:73–74

    Google Scholar 

  • Lindner DL, Banik MT (2011) Intragenomic variation in the ITS rDNA region obscures phylogenetic relationships and inflates estimates of operational taxonomic units in genus Laetiporus. Mycologia 103:731–740

    Article  PubMed  Google Scholar 

  • Link JHF (1833) Amanita ovoidea (Bull.) Link. Handb Erk Gew 3:273

    Google Scholar 

  • Loizides M, Bellanger JM, Yiangou Y, Moreau PA (2018) Preliminary phylogenetic investigations into the genus Amanita (Agaricales) in Cyprus, with a review of previous records and poisoning incidents. Doc mycol XXXVII, p 201–218

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: gateway computing environments workshop 2010 (GCE), 2010. IEEE:1–8

  • Neville P, Poumarat S (2004) Amaniteae. 1. Fungi Europaei 9:1–1119

  • Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinforma 4:193–201

    Article  Google Scholar 

  • Paolocci F, Rubini A, Granetti B, Arcioni S (1999) Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizae. FEMS Microbiol Ecol 28:23–30

    Article  CAS  Google Scholar 

  • Pelizzari V, Moser M (1999) Non-protein amino-acids as toxic principle in species of Amanita. In: Atti del 1° Convegno Internazionale di Micotossicologia. Pagine di Micologia 11:99–104

    Google Scholar 

  • Pelizzari V, Feifel E, Rohrmoser MM, Gstraunthaler G, Moser M (1994) Partial purification and characterization of a toxic component of Amanita smithiana. Mycologia 86:555–560

    Article  CAS  Google Scholar 

  • Redhead SA, Vizzini A, Drehmel DC, Contu M (2016) Saproamanita, a new name for both Lepidella E.-J. Gilbert and Aspidella E.-J. Gilbert (Amanitae, Amanitaceae). IMA Fungus 7:119–129

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, H ̈ohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2011) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a largemodel space. Syst Biol 61:539–542

    Article  Google Scholar 

  • Rubini A, Paolocci F, Granetti B, Arcioni S (1998) Single step molecular characterization of morphologically similar black truffle species. FEMS Microbiol Lett 164:7–12

    Article  CAS  Google Scholar 

  • Saviuc P, Danel V (2006) New syndromes in mushroom poisoning. Toxicol Rev 25:199–209

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traverso M (1998) Il genere Amanita in Italia. AMER, Roma

  • Tulloss RE (2000) Note sulla metodologia per lo studio del genere Amanita (Agaricales). Boll Gruppo Micol G Bresadola 43:41–58

    Google Scholar 

  • Tulloss RE, Lindgren JE (1992) Amanita smithiana: taxonomy, distribution and poisonings. Mycotaxon 45:373–387

    Google Scholar 

  • Tulloss RE, Rodríguez Caycedo C (2011) Amanita workshop, 6th ed. amanitabear.com and amanitaceae.org Roosevelt, New Jersey

  • Tulloss RE, Rodríguez-Caycedo C, Hughes KW, Geml J, Kudzma LV, Wolfe BE, Arora D (2015) Nomenclatural changes in Amanita II. Amanitaceae 1:1–6

    Google Scholar 

  • Tulloss RE, Kuyper TW, Vellinga EC, Yang ZL, Halling RE, Geml J, Sánchez-Ramírez S, Gonçalves SC, Hess J, Pringle A (2016) The genus Amanita should not be split. Amanitaceae 1:1–16

    Google Scholar 

  • Vellinga EC, Kuyper TW, Ammirati J, Desjardin DE, Halling RE, Justo A, Læssøe T, Lebel T, Lodge DJ, Matheny PB, Methven AS, Moreau PA, Mueller GM, Noordeloos ME, Nuytick J, Ovrebo CL, Verbeken A (2015) Six simple guidelines for introducing new genera of fungi. IMA Fungus 6:65–68

    Article  Google Scholar 

  • Weiß M, Yang ZL, Oberwinkler F (1998) Molecular phylogenetic studies in the genus Amanita. Can J Bot 76:1170–1179

    Google Scholar 

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

    Google Scholar 

  • Wolfe BE, Tulloss RE, Pringle A (2012) The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS One 7:e39597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZL (1997) Die Amanita-Arten von Suedwestchina. Bibl Mycol 170:1–240

    Google Scholar 

  • Zhang LF, Yang JB, Yang ZL (2004) Molecular phylogeny of eastern Asian species of Amanita (Agaricales, Basidiomycota): taxonomic and biogeographic implications. Fungal Divers 17:219–238

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Elena Salerni, Lisa Martelli, and Diego Cantini for their collaboration and Salvatore Curreli, Emidio Borghi, and Ursula Peintner for providing fruiting bodies and express their gratitude to Dr. Denis Benjamin for assisting with citations of literature.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudia Riccioni.

Additional information

Section Editor: Zhu-Liang Yang

Publisher’s note

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

Electronic supplementary material

ESM 1

Supplementary Figures (PDF 2134 kb)

ESM 2

Supplementary Table (XLS 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Riccioni, C., Paolocci, F., Tulloss, R.E. et al. Molecular phylogenetic analyses show that Amanita ovoidea and Amanita proxima are distinct species and suggest their assignment to Roanokenses section. Mycol Progress 18, 1275–1283 (2019). https://doi.org/10.1007/s11557-019-01521-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-019-01521-2

Keywords