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Drosophila, destroying angels, and deathcaps! Oh my! A review of mycotoxin tolerance in the genus Drosophila

  • Review
  • Published:
Frontiers in Biology

Abstract

Background

Evolutionary novelties, be they morphological or biochemical, fascinate both scientists and non-scientists alike. These types of adaptations can significantly impact the biodiversity of the organisms in which they occur. While much work has been invested in the evolution of novel morphological traits, substantially less is known about the evolution of biochemical adaptations.

Methods

In this review, we present the results of literature searches relating to one such biochemical adaptation: α-amanitin tolerance/resistance in the genus Drosophila.

Results

Amatoxins, including α-amanitin, are one of several toxin classes found in Amanita mushrooms. They act by binding to RNA polymerase II and inhibiting RNA transcription. Although these toxins are lethal to most eukaryotic organisms, 17 mushroom-feeding Drosophila species are tolerant of natural concentrations of amatoxins and can develop in toxic mushrooms. The use of toxic mushrooms allows these species to avoid infection by parasitic nematodes and lowers competition. Their amatoxin tolerance is not due to mutations that would inhibit α-amanitin from binding to RNA polymerase II. Furthermore, the mushroom-feeding flies are able to detoxify the other toxin classes that occur in their mushroom hosts. In addition, resistance has evolved independently in several D. melanogaster strains. Only one of the strains exhibits resistance due to mutations in the target of the toxin.

Conclusions

Given our current understanding of the evolutionary relationships among the mushroom-feeding flies, it appears that amatoxin tolerance evolved multiple times. Furthermore, independent lines of evidence suggest that multiple mechanisms confer α-amanitin tolerance/resistance in Drosophila.

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References

  • Amichot M, Tarès S, Brun-Barale A, Arthaud L, Bride J M, Bergé J B (2004). Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism. Eur J Biochem, 271(7): 1250–1257

    Article  PubMed  CAS  Google Scholar 

  • Begun D J, Whitley P (2000). Genetics of α-amanitin resistance in a natural population of Drosophila melanogaster. Heredity (Edinb), 85 (Pt 2): 184–190

    Article  CAS  Google Scholar 

  • Berger K J, Guss D A (2005a). Mycotoxins revisited: Part I. J Emerg Med, 28(1): 53–62

    Article  PubMed  Google Scholar 

  • Berger K J, Guss D A (2005b). Mycotoxins revisited: Part II. J EmergMed, 28(2): 175–183

    Article  Google Scholar 

  • Beutler J A, Der Marderosian A H (1981). Chemical variation in Amanita. J Nat Prod, 44(4): 422–431

    Article  CAS  Google Scholar 

  • Bosman C K, Berman L, Isaacson M, Wolfowitz B, Parkes J (1965). Mushroom poisoning caused by Amanita pantherina. Report of 4 cases. S Afr Med J, 39(39): 983–986

    PubMed  CAS  Google Scholar 

  • Bray M J, Werner T, Dyer K A (2014). Two genomic regions together cause dark abdominal pigmentation in Drosophila tenebrosa. Heredity (Edinb), 112(4): 454–462

    Article  CAS  Google Scholar 

  • Bresinsky A, Besl H (1990) A color atlas of poisonous fungi: a handbook for pharmacists, doctors and biologists.Wolfe, Wurzburg, Germany, 295 pp.

    Google Scholar 

  • Broeckhoven C, Diedericks G, Hui C, Makhubo B G, Mouton P L (2016). Enemy at the gates: Rapid defensive trait diversification in an adaptive radiation of lizards. Evolution, 70(11): 2647–2656

    Article  PubMed  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Green J, Rumack B H, Heard S E (2007). 2006 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS). Clin Toxicol (Phila), 45(8): 815–917

    Article  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Green J L, Rumack B H, Dart R C (2011). 2010 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 28th Annual Report. Clin Toxicol (Phila), 49(10): 910–941

    Article  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Green J L, Rumack B H, Giffin S L (2009). 2008 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 26th Annual Report. Clin Toxicol (Phila), 47(10): 911–1084

    Article  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Green J L, Rumack B H, Giffin S L (2010). 2009 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 27th Annual Report. Clin Toxicol (Phila), 48(10): 979–1178

    Article  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Green J L, Rumack B H, Heard S E, and the American Association of Poison Control Centers (2008). 2007 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 25th Annual Report. Clin Toxicol (Phila), 46(10): 927–1057

    Article  Google Scholar 

  • Bronstein A C, Spyker D A, Cantilena L R Jr, Rumack B H, Dart R C (2012). 2011 Annual report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 29th Annual Report. Clin Toxicol (Phila), 50(10): 911–1164

    Article  Google Scholar 

  • Broussard C N, Aggarwal A, Lacey S R, Post A B, Gramlich T, Henderson J M, Younossi Z M (2001). Mushroom poisoning–from diarrhea to liver transplantation. Am J Gastroenterol, 96(11): 3195–3198

    PubMed  CAS  Google Scholar 

  • Brun A, Cuany A, Le Mouel T, Berge J, Amichot M (1996). Inducibility of the Drosophila melanogaster cytochrome P450 gene, CYP6A2, by phenobarbital in insecticide susceptible or resistant strains. Insect Biochem Mol Biol, 26(7): 697–703

    Article  PubMed  CAS  Google Scholar 

  • Bushnell D A, Cramer P, Kornberg R D (2002). Structural basis of transcription: α-amanitin-RNA polymerase II cocrystal at 2.8 A resolution. Proc Natl Acad Sci USA, 99(3): 1218–1222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Buxton P A (1960). British Diptera associated with fungi. III. Flies of all families reared from about 150 species of fungi. Entomol Mon Mag, 96: 61–94

    Google Scholar 

  • Chambers T C, McAvoy E M, Jacobs J W, Eilon G (1990). Protein kinase C phosphorylates P-glycoprotein in multidrug resistant human KB carcinoma cells. J Biol Chem, 265(13): 7679–7686

    PubMed  CAS  Google Scholar 

  • Chang S T, Miles P G (2004) Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact. CRC Press, Boca Raton, FL, 451 pp.

    Google Scholar 

  • Chilton W S, Ott J (1976). Toxic metabolites of Amanita pantherina, A. cothurnata, A. muscaria and other Amanita species. Lloydia, 39(2-3): 150–157

    PubMed  CAS  Google Scholar 

  • Coyne J A, Orr H A (2004) Speciation. Sinauer Associates, Inc., Sunderland, Massachusetts, 545 pp.

    Google Scholar 

  • Daborn P J, Lumb C, Boey A, Wong W, Ffrench-Constant R H, Batterham P (2007). Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem Mol Biol, 37(5): 512–519

    Article  PubMed  CAS  Google Scholar 

  • Debban C L, Dyer K A (2013). No evidence for behavioural adaptations to nematode parasitism by the fly Drosophila putrida. J Evol Biol, 26 (8): 1646–1654

    Article  PubMed  CAS  Google Scholar 

  • Diaz J H (2005). Syndromic diagnosis and management of confirmed mushroom poisonings. Crit Care Med, 33(2): 427–436

    Article  PubMed  Google Scholar 

  • Duensing A, Liu Y, Spardy N, Bartoli K, Tseng M, Kwon J A, Teng X, Duensing S (2007). RNA polymerase II transcription is required for human papillomavirus type 16 E7- and hydroxyurea-induced centriole overduplication. Oncogene, 26(2): 215–223

    Article  PubMed  CAS  Google Scholar 

  • Dyer K A, Bray M J, Lopez S J (2013). Genomic conflict drives patterns of X-linked population structure in Drosophila neotestacea. Mol Ecol, 22(1): 157–169

    Article  PubMed  Google Scholar 

  • Dyer K A, Burke C, Jaenike J (2011). Wolbachia-mediated persistence of mtDNA from a potentially extinct species. Mol Ecol, 20(13): 2805–2817

    Article  PubMed  Google Scholar 

  • Dyer K A, Charlesworth B, Jaenike J (2007). Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proc Natl Acad Sci USA, 104(5): 1587–1592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dyer K A, Jaenike J (2005). Evolutionary dynamics of a spatially structured host-parasite association: Drosophila innubila and malekilling Wolbachia. Evolution, 59(7): 1518–1528

    Article  PubMed  Google Scholar 

  • Emlen D J (2000). Integrating development with evolution: a case study with beetle horns: results from studies of the mechanisms of horn development shed new light on our understanding of beetle horn evolution. BioSciences, 50(5): 403–418

    Article  Google Scholar 

  • Enjalbert F, Gallion C, Jehl F, Monteil H (1993). Toxin content, phallotoxin and amatoxin composition of Amanita phalloides tissues. Toxicon, 31(6): 803–807

    Article  PubMed  CAS  Google Scholar 

  • Enjalbert F, Rapior S, Nouguier-Soulé J, Guillon S, Amouroux N, Cabot C (2002). Treatment of amatoxin poisoning: 20-year retrospective analysis. J Toxicol Clin Toxicol, 40(6): 715–757

    Article  PubMed  CAS  Google Scholar 

  • Erden A, Esmeray K, Karagöz H, Karahan S, Gümüşçü H H, Başak M, Cetinkaya A, Avcı D, Poyrazoğlu O K (2013). Acute liver failure caused by mushroom poisoning: a case report and review of the literature. Int Med Case Rep J, 6: 85–90

    PubMed  PubMed Central  Google Scholar 

  • Escudié L, Francoz C, Vinel J P, Moucari R, Cournot M, Paradis V, Sauvanet A, Belghiti J, Valla D, Bernuau J, Durand F (2007). Amanita phalloides poisoning: reassessment of prognostic factors and indications for emergency liver transplantation. J Hepatol, 46(3): 466–473

    Article  PubMed  Google Scholar 

  • Faulstich H (1980). Mushroom poisoning. Lancet, 2(8198): 794–795

    Article  PubMed  CAS  Google Scholar 

  • Faulstich H, Cochet-Meilhac M (1976). Amatoxins in edible mushrooms. FEBS Lett, 64(1): 73–75

    Article  PubMed  CAS  Google Scholar 

  • Festucci-Buselli R A, Carvalho-Dias A S, de Oliveira-Andrade M, Caixeta-Nunes C, Li H M, Stuart J J, Muir W, Scharf M E, Pittendrigh B R (2005). Expression of Cyp6g1 and Cyp12d1 in DDT resistant and susceptible strains of Drosophila melanogaster. Insect Mol Biol, 14(1): 69–77

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Nabholz B, Glémin S, Hurst G D (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol, 18(22): 4541–4550

    Article  PubMed  CAS  Google Scholar 

  • Garcia J, Carvalho A T, Dourado D F, Baptista P, de Lourdes Bastos M, Carvalho F (2014). New in silico insights into the inhibition of RNAP II by α-amanitin and the protective effect mediated by effective antidotes. J Mol Graph Model, 51: 120–127

    Article  PubMed  CAS  Google Scholar 

  • Gleixner E M, Canaud G, Hermle T, Guida M C, Kretz O, Helmstädter M, Huber T B, Eimer S, Terzi F, SimonsM(2014). V-ATPase/mTOR signaling regulates megalin-mediated apical endocytosis. Cell Reports, 8(1): 10–19

    Article  PubMed  CAS  Google Scholar 

  • Greenleaf A L, Borsett L M, Jiamachello P F, Coulter D E (1979). α-amanitin-resistant D. melanogaster with an altered RNA polymerase II. Cell, 18(3): 613–622

    Article  PubMed  CAS  Google Scholar 

  • Grimaldi D (1985). Niche separation and competitive coexistence in mycophagous Drosophila (Diptera: Drosophilidae). Proc Entomol Soc Wash, 87: 498–511

    Google Scholar 

  • Grimaldi D, Jaenike J (1984). Competition in natural populations of mycophagous Drosophila. Ecology, 65(4): 1113–1120

    Article  Google Scholar 

  • Hackman W, Meinander M (1979). Diptera feeding as larvae on macrofungi in Finland. Ann Zool Fenn, 16: 50–83

    Google Scholar 

  • Hallen H E, Adams G C, Eicker A, Jäger A K (2002). Amatoxins and phallotoxins in indigenous and introduced South African Amanita species. S Afr J Bot, 68(3): 322–326

    Article  CAS  Google Scholar 

  • Hallen H E, Luo H, Scott-Craig J S, Walton J D (2007). Gene family encoding the major toxins of lethal Amanita mushrooms. Proc Natl Acad Sci USA, 104(48): 19097–19101

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatadani L M, McInerney J O, de Medeiros H F, Junqueira A C, de Azeredo-Espin A M, Klaczko L B (2009). Molecular phylogeny of the Drosophila tripunctata and closely related species groups (Diptera: Drosophilidae). Mol Phylogenet Evol, 51(3): 595–600

    Article  PubMed  CAS  Google Scholar 

  • Heard S B, Hauser D L (1995). Key evolutionary innovations and their ecological mechanisms. Hist Biol, 10(2): 151–173

    Article  Google Scholar 

  • Huang W, Massouras A, Inoue Y, Peiffer J, Ràmia M, Tarone A M, Turlapati L, Zichner T, Zhu D, Lyman R F, Magwire M M, Blankenburg K, Carbone MA, Chang K Ellis L L, Fernandez S, Han Y, Highnam G, Hjelmen C E, Jack J R, Javaid M, Jayaseelan J, Kalra D, Lee S, Lewis L, Munidasa M, Ongeri F, Patel S, Perales L, Perez A, Pu L, Rollmann S M, Ruth R, Saada N, Warner C, Williams A, Wu Y Q, Yamamoto A, Zhang Y, Zhu Y, Anholt R R, Korbel J O, Mittelman D, Muzny D M, Gibbs R A, Barbadilla A, Johnston J S, Stone E A, Richards S, Deplancke B, Mackay T F (2014). Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res, 24(7): 1193–1208

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Humphreys D P, Rundle H D, Dyer K A (2016). Patterns of reproductive isolation in the Drosophila subquinariacomplex: can reinforced premating isolation cascade to other species? Curr Zool, 62(2): 183–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Hurst G D D, Jiggins F M (2005). Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc Biol Sci, 272(1572): 1525–1534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Izumitani H F, Kusaka Y, Koshikawa S, Toda M J, Katoh T (2016). Phylogeography of the subgenus Drosophila (Diptera: Drosophilidae): evolutionary history of faunal divergence between the old and the new worlds. PLoS One, 11(7): e0160051

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaenike J (1978a). Host selection by mycophagous Drosophila. Ecology, 59(6): 1286–1288

    Article  Google Scholar 

  • Jaenike J (1978b). Resource predictability and niche breadth in the Drosophila quinaria species group. Evolution, 32(3): 676–678

    Article  PubMed  Google Scholar 

  • Jaenike J (1985a). Genetic and environmental determinants of food preference in Drosophila tripunctata. Evolution, 39(2): 362–369

    Article  PubMed  Google Scholar 

  • Jaenike J (1985b). Parasite pressure and the evolution of amanitin tolerance in Drosophila. Evolution, 39(6): 1295–1301

    Article  PubMed  Google Scholar 

  • Jaenike J (1986). Genetic complexity of host-selection behavior in Drosophila. Proc Natl Acad Sci USA, 83(7): 2148–2151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaenike J (1987). Genetics of oviposition-site preference in Drosophila tripunctata. Heredity (Edinb), 59(Pt 3): 363–369

    Article  Google Scholar 

  • Jaenike J (1989). Genetic population structure of Drosophila tripunctata: Patterns of varitation and covariation of traits affecting resource use. Evolution, 43(7): 1467–1482

    PubMed  Google Scholar 

  • Jaenike J (1992). Mycophagous Drosophila and their nematode parasites. Am Nat, 139(5): 893–906

    Article  Google Scholar 

  • Jaenike J, Dyer K A, Cornish C, Minhas M S (2006). Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol, 4 (10): e325

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaenike J, Grimaldi D (1983). Genetic variation for host preference within and among populations of Drosophila tripunctata. Evolution, 37(5): 1023–1033

    Article  PubMed  Google Scholar 

  • Jaenike J, Grimaldi D A, Sluder A E, Greenleaf A L (1983). a-Amanitin tolerance in mycophagous Drosophila. Science, 221(4606): 165–167

    Article  PubMed  CAS  Google Scholar 

  • Jaenike J, James A C (1991). Aggregation and the coexistence of mycophagous Drosophila. J Anim Ecol, 60(3): 913–928

    Article  Google Scholar 

  • Jaenike J, Perlman S J (2002). Ecology and evolution of host-parasite associations: mycophagous Drosophila and their parasitic nematodes. Am Nat, 160(Suppl 4): S23–S39

    PubMed  Google Scholar 

  • Jaenike J, Selander R K (1979). Ecological generalism in Drosophila falleni: genetic evidence. Evolution, 33(2): 741–748

    Article  PubMed  Google Scholar 

  • Kalač P (2009). Chemical composition and nutritional value of European species of wild growing mushrooms: a review. Food Chem, 113(1): 9–16

    Article  CAS  Google Scholar 

  • Kalač P (2013). A review of chemical composition and nutritional value of wild-growing and cultivated mushrooms. J Sci Food Agric, 93(2): 209–218

    Article  PubMed  CAS  Google Scholar 

  • Kalajdzic P, Oehler S, Reczko M, Pavlidi N, Vontas J, Hatzigeorgiou A G, Savakis C (2012). Use of mutagenesis, genetic mapping and next generation transcriptomics to investigate insecticide resistance mechanisms. PLoS One, 7(6): e40296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaplan C D, Larsson K M, Kornberg R D (2008). The RNA polymerase II trigger loop functions in substrate selection and is directly targeted by α-amanitin. Mol Cell, 30(5): 547–556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karlson-Stiber C, Persson H (2003). Cytotoxic fungi–an overview. Toxicon, 42(4): 339–349

    Article  PubMed  CAS  Google Scholar 

  • Kaul T N (2002) Biology and conservation of mushrooms. Science Publishers, Inc., Enfield (NH), USA, 255 pp.

    Google Scholar 

  • Kaya E, Karahan S, Bayram R, Yaykasli K O, Colakoglu S, Saritas A (2015). Amatoxin and phallotoxin concentration in Amanita phalloides spores and tissues. Toxicol Ind Health, 31(12): 1172–1177

    Article  PubMed  CAS  Google Scholar 

  • Kaya E, Yilmaz I, Sinirlioglu Z A, Karahan S, Bayram R, Yaykasli K O, Colakoglu S, Saritas A, Severoglu Z (2013). Amanitin and phallotoxin concentration in Amanita phalloides var. alba mushroom. Toxicon, 76: 225–233

    Article  PubMed  CAS  Google Scholar 

  • Kijimoto T, Moczek A P, Andrews J (2012). Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc Natl Acad Sci USA, 109(50): 20526–20531

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim Y C, Guan K L (2015). mTOR: a pharmacologic target for autophagy regulation. J Clin Invest, 125(1): 25–32

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura M T (1980). Evolution of food preferences in fungus-feeding Drosophila: an ecological study. Evolution, 34(5): 1009–1018

    PubMed  Google Scholar 

  • Kimura M T, Toda M J (1989). Food preferences and nematode parasitism in mycophagous Drosophila. Ecol Res, 4(2): 209–218

    Article  Google Scholar 

  • Kume K, Ikeda M, Miura S, Ito K, Sato K A, Ohmori Y, Endo F, Katagiri H, Ishida K, Ito C, Iwaya T, Nishizuka S S (2016). α-Amanitin Restrains Cancer Relapse from Drug-Tolerant Cell Subpopulations via TAF15. Sci Rep, 6(1): 25895

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lacy R C (1984). Predictability, toxicity, and trophic niche breadth in fungus-feeding Drosophilidae (Diptera). Ecol Entomol, 9(1): 43–54

    Article  Google Scholar 

  • Lai M W, Klein-Schwartz W, Rodgers G C Jr, Abrams J Y, Haber D A, Bronstein A C, Wruk K M (2006). 2005 Annual Report of the American Association of Poison Control Centers’ national poisoning and exposure database. Clin Toxicol (Phila), 44(6-7): 803–932

    Article  CAS  Google Scholar 

  • Le Goff G, Hilliou F, Siegfried B D, Boundy S, Wajnberg E, Sofer L, Audant P, ffrench-Constant R H, Feyereisen R (2006). Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and GST gene induction. Insect Biochem Mol Biol, 36(8): 674–682

    Article  PubMed  CAS  Google Scholar 

  • Leathem A M, Purssell R A, Chan V R, Kroeger P D (1997). Renal failure caused by mushroom poisoning. J Toxicol Clin Toxicol, 35 (1): 67–75

    Article  PubMed  CAS  Google Scholar 

  • Li C, Oberlies N H (2005). The most widely recognized mushroom: chemistry of the genus Amanita. Life Sci, 78(5): 532–538

    Article  PubMed  CAS  Google Scholar 

  • Lindell T J, Weinberg F, Morris P W, Roeder R G, Rutter W J (1970). Specific inhibition of nuclear RNA polymerase II by α-amanitin. Science, 170(3956): 447–449

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Felberg L, Soloway R A, Ford M, Geller R (1995). 1994 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 13(5): 551–597

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Felberg L, White S, Klein-Schwartz W (1996). 1995 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 14(5): 487–537

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Klein-Schwartz W, Caravati E M, Youniss J, Crouch B, Lee S (1999). 1998 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 17(5): 435–487

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Klein-Schwartz W, Dyer K S, Shannon M, Lee S, Powers M (1998). 1997 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 16(5): 443–497

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Klein-Schwartz W, Rodgers G C Jr, Cobaugh D J, Youniss J, Omslaer J C, May M E, Woolf A D, Benson B E (2002). 2001 Annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 20(5): 391–452

    Article  PubMed  Google Scholar 

  • Litovitz T L, Klein-Schwartz W, White S, Cobaugh D J, Youniss J, Drab A, Benson B E (2000). 1999 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 18(5): 517–574

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Klein-Schwartz W, White S, Cobaugh D J, Youniss J, Omslaer J C, Drab A, Benson B E (2001). 2000 Annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 19(5): 337–395

    Article  PubMed  CAS  Google Scholar 

  • Litovitz T L, Smilkstein M, Felberg L, Klein-Schwartz W, Berlin R, Morgan J L (1997). 1996 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 15(5): 447–500

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhang X, Han C, Wan G, Huang X, Ivan C, Jiang D, Rodriguez-Aguayo C, Lopez-Berestein G, Rao P H, Maru D M, Pahl A, He X, Sood A K, Ellis L M, Anderl J, Lu X (2015). TP53 loss creates therapeutic vulnerability in colorectal cancer. Nature, 520(7549): 697–701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mackay T F, Richards S, Stone E A, Barbadilla A, Ayroles J F, Zhu D, Casillas S, Han Y, Magwire M M, Cridland J M, Richardson M F, Anholt R R, Barrón M, Bess C, Blankenburg K P, Carbone M A, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan J C, Jhangiani S N, Jordan K W, Lara F, Lawrence F, Lee S L, Librado P, Linheiro R S, Lyman R F, Mackey A J, Munidasa M, Muzny D M, Nazareth L, Newsham I, Perales L, Pu L L, Qu C, Ràmia M, Reid J G, Rollmann S M, Rozas J, Saada N, Turlapati L, Worley K C, Wu Y Q, Yamamoto A, Zhu Y, Bergman C M, Thornton K R, Mittelman D, Gibbs R A (2012). The Drosophila melanogaster Genetic Reference Panel. Nature, 482(7384): 173–178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marciniak B, Łopaczyńska D, Ferenc T (2017). Evaluation of the genotoxicity of alpha-amanitin in mice bone marrow cells. Toxicon, 137: 1–6

    Article  PubMed  CAS  Google Scholar 

  • Mas A (2005). Mushrooms, amatoxins and the liver. J Hepatol, 42(2): 166–169

    Article  PubMed  Google Scholar 

  • Mitchell C L, Latuszek C E, Vogel K R, Greenlund I M, Hobmeier R E, Ingram O K, Dufek S R, Pecore J L, Nip F R, Johnson Z J, Ji X, Wei H, Gailing O, Werner T (2017). a-amanitin resistance in Drosophila melanogaster: A genome-wide association approach. PLoS One, 12 (2): e0173162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell C L, Saul M C, Lei L, Wei H, Werner T (2014). The mechanisms underlying α-amanitin resistance in Drosophila melanogaster: a microarray analysis. PLoS One, 9(4): e93489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell C L, Yeager R D, Johnson Z J, D’Annunzio S E, Vogel K R, Werner T (2015). Long-term resistance of Drosophila melanogaster to the mushroom toxin α-amanitin. PLoS One, 10(5): e0127569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moldenhauer G, Salnikov A V, Lüttgau S, Herr I, Anderl J, Faulstich H (2012). Therapeutic potential of amanitin-conjugated anti-epithelial cell adhesion molecule monoclonal antibody against pancreatic carcinoma. J Natl Cancer Inst, 104(8): 622–634

    Article  PubMed  CAS  Google Scholar 

  • Morales-Hojas R, Vieira J (2012). Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. PLoS One, 7(11): e49552

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moshnikova A, Moshnikova V, Andreev O A, Reshetnyak Y K (2013). Antiproliferative effect of pHLIP-amanitin. Biochemistry, 52(7): 1171–1178

    Article  PubMed  CAS  Google Scholar 

  • Mowry J B, Spyker D A, Cantilena L R Jr, Bailey J E, Ford M (2013). 2012 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 30th Annual Report. Clin Toxicol (Phila), 51(10): 949–1229

    Article  CAS  Google Scholar 

  • Mowry J B, Spyker D A, Cantilena L R Jr, McMillan N, Ford M (2014). 2013 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 31st Annual Report. Clin Toxicol (Phila), 52(10): 1032–1283

    Article  Google Scholar 

  • Obodai M, Ferreira I C F R, Fernandes A, Barros L, Mensah D L N, Dzomeku M, Urben A F, Prempeh J, Takli R K (2014). Evaluation of the chemical and antioxidant properties of wild and cultivated mushrooms of Ghana. Molecules, 19(12): 19532–19548

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Perlman S J, Jaenike J (2003). Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution, 57(3): 544–557

    Article  PubMed  Google Scholar 

  • Perlman S J, Spicer G S, Shoemaker D D, Jaenike J (2003). Associations between mycophagous Drosophila and their Howardula nematode parasites: a worldwide phylogenetic shuffle. Mol Ecol, 12(1): 237–249

    Article  PubMed  CAS  Google Scholar 

  • Phillips J P, Willms J, Pitt A (1982). α-amanitin resistance in three wild strains of Drosophila melanogaster. Can J Genet Cytol, 24(2): 151–162

    Article  PubMed  CAS  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press Inc., Oxford, New York.

    Google Scholar 

  • Shoemaker D D, Katju V, Jaenike J (1999). Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution, 53(4): 1157–1164

    Article  PubMed  Google Scholar 

  • Shorrocks B, Charlesworth P (1980). The distribution and abundance of the British fungal-breeding Drosophila. Ecol Entomol, 5(1): 61–78

    Article  Google Scholar 

  • Shorrocks B, Wood A M (1973). A preliminary note on the fungus feeding species of Drosophila. J Nat Hist, 7(5): 551–556

    Article  Google Scholar 

  • Simpson G G (1953) The major features of evolution. Columbia University Press, New York, New York.

    Google Scholar 

  • Spicer G S, Jaenike J (1996). PHYLOGENETIC ANALYSIS OF BREEDING SITE USE AND α-AMANITIN TOLERANCE WITHIN THE DROSOPHILA QUINARIA SPECIES GROUP. Evolution, 50(6): 2328–2337

    PubMed  Google Scholar 

  • Stansbury M S, Moczek A P (2014). The function of Hox and appendage-patterning genes in the development of an evolutionary novelty, the Photuris firefly lantern. Proc Biol Sci, 281(1782): 20133333

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stump A D, Jablonski S E, Bouton L, Wilder J A (2011). Distribution and mechanism of α-amanitin tolerance in mycophagous Drosophila (Diptera: Drosophilidae). Environ Entomol, 40(6): 1604–1612

    Article  PubMed  CAS  Google Scholar 

  • Toledo C V, Barroetaveña C, Fernandes Â, Barros L, Ferreira I C F R (2016). Chemical and antioxidant properties of wild edible mushrooms from native Nothfagus spp. forest, Argentina. Molecules, 21 (9): 1201

    Article  CAS  PubMed Central  Google Scholar 

  • Tuno N, Takahashi K H, Yamashita H, Osawa N, Tanaka C (2007). Tolerance of Drosophila flies to ibotenic acid poisons in mushrooms. J Chem Ecol, 33(2): 311–317

    Article  PubMed  CAS  Google Scholar 

  • Tyler V E Jr, Benedict R G, Brady L R, Robbers J E (1966). Occurrence of Amanita toxins in American collections of deadly amanitas. J Pharm Sci, 55(6): 590–593

    Article  PubMed  CAS  Google Scholar 

  • Vetter J (1998). Toxins of Amanita phalloides. Toxicon, 36(1): 13–24

    Article  PubMed  CAS  Google Scholar 

  • Walton J D, Hallen-Adams H E, Luo H (2010). Ribosomal biosynthesis of the cyclic peptide toxins of Amanita mushrooms. Biopolymers, 94 (5): 659–664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watson W A, Litovitz T L, Klein-Schwartz W, Rodgers G C Jr, Youniss J, Reid N, Rouse W G, Rembert R S, Borys D (2004). 2003 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 22(5): 335–404

    Article  PubMed  Google Scholar 

  • Watson W A, Litovitz T L, Rodgers G C Jr, Klein-Schwartz W, Reid N, Youniss J, Flanagan A, Wruk K M (2005). 2004 Annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 23(5): 589–666

    Article  PubMed  Google Scholar 

  • Watson W A, Litovitz T L, Rodgers G C Jr, Klein-Schwartz W, Youniss J, Rose S R, Borys D, May M E (2003). 2002 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med, 21(5): 353–421

    Article  PubMed  Google Scholar 

  • Werner T (2017). The Drosophilids of a pristine old-growth northern hardwood forest. Great Lakes Entomol, 50: 68–78

    Google Scholar 

  • Werner T, Jaenike J (2017) Drosophilids of the Midwest and Northeast. River Campus Libraries, University of Rochester, Rochester, NY, 256 pp.

    Google Scholar 

  • Werren J H, Jaenike J (1995). Wolbachia and cytoplasmic incompatibility in mycophagous Drosophila and their relatives. Heredity (Edinb), 75(Pt 3): 320–326

    Article  Google Scholar 

  • Wieland T (1968). Poisonous principles of mushrooms of the genus Amanita. Four-carbon amines acting on the central nervous system and cell-destroying cyclic peptides are produced. Science, 159 (3818): 946–952

    PubMed  CAS  Google Scholar 

  • Wieland T (1983). The toxic peptides from Amanita mushrooms. Int J Pept Protein Res, 22(3): 257–276

    Article  PubMed  CAS  Google Scholar 

  • Wieland T (1986). Peptides of poisonous Amanita mushrooms. Springer-Verlag, New York, 256 pp.

    Book  Google Scholar 

  • Wieland T, Faulstich H, Fiume L (1978). Amatoxins, phallotoxins, phallolysin, and antamanide: the biologically active components of poisonous Amanita mushrooms. CRC Crit Rev Biochem, 5(3): 185–260

    Article  PubMed  CAS  Google Scholar 

  • Yocum R R, Simons D M (1977). Amatoxins and phallotoxins in Amanita species of the Northeastern United States. Lloydia, 40: 178–190

    PubMed  CAS  Google Scholar 

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Acknowledgements

This review was supported by an NSF grant Laura Reed and CSC and an NSF grant DEB-1737877 to TW.We would like to thank Kelly Dyer and Laura Reed for constructive discussions regarding the natural history of mushroom-feeding Drosophila, toxin tolerance, and the evolutionary relationships among these species. We would also like to thank Prajakta Kokate, Pablo Chialvo, and members of the Reed Laboratory for critical reviews of the manuscript.

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  1. Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama, USA

    Clare H. Scott Chialvo

  2. Department of Biological Sciences, Michigan Technological University, Houghton, Michigan, USA

    Thomas Werner

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Scott Chialvo, C.H., Werner, T. Drosophila, destroying angels, and deathcaps! Oh my! A review of mycotoxin tolerance in the genus Drosophila. Front. Biol. 13, 91–102 (2018). https://doi.org/10.1007/s11515-018-1487-1

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