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Front. Biol.    2018, Vol. 13 Issue (2) : 91-102    https://doi.org/10.1007/s11515-018-1487-1
REVIEW
Drosophila, destroying angels, and deathcaps! Oh my! A review of mycotoxin tolerance in the genus Drosophila
Clare H. Scott Chialvo1(), Thomas Werner2()
1. Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama, USA
2. Department of Biological Sciences, Michigan Technological University, Houghton, Michigan, USA
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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.
Keywords Drosophila      mushroom-feeding      biochemical adaptations      mushroom toxins      cyclopeptides      α-amanitin     
Corresponding Author(s): Clare H. Scott Chialvo,Thomas Werner   
Online First Date: 24 April 2018    Issue Date: 28 May 2018
 Cite this article:   
Clare H. Scott Chialvo,Thomas Werner. Drosophila, destroying angels, and deathcaps! Oh my! A review of mycotoxin tolerance in the genus Drosophila[J]. Front. Biol., 2018, 13(2): 91-102.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-018-1487-1
https://academic.hep.com.cn/fib/EN/Y2018/V13/I2/91
Phase Onset Symptoms
Latent 0-12 h Asymptomatic
Gastrointestinal ?Distress 6-24 h Abdominal pain, vomiting, diarrhea
Apparent ?Convalescence 24-72 h Asymptomatically rising liver enzymes
Hepatic 3-9 days Hepatic and renal failure, coma, death
Tab.1  Four phases of cyclopeptide poisoning (Berger and Guss, 2005a; Diaz, 2005; Mas, 2005)
Group Species Host sites α-amanitin
concentrations (µg/mL) a		 Ibotenic acid concentrations (µg/mL)b
5 10 50 50c 50d 62.5 125 250 500
quinaria brachynephros M – – N – – N N N N
phalerata M – – N L SD – – – –
falleni M – – SD N – – – – –
angularis M – – N N N N N N N
deflecta V – – D – – – – – –
recens M N N N L – – – – –
quinaria V – – D – – – – – –
subquinaria M – – N – – – – – –
nigromaculata M, V, F – – N N N – – – –
guttifera M – – SD N N – – – –
tripunctata tripunctata M, F N N SD,Ne – – – – – –
cardini cardini M, F – – N SD SI – – – –
acutilabella M, F – – N L N – – – –
testacea putrida M N N SI – – – – – –
bizonata bizonata M – – – – – – – – N
immigrans immigrans F, M N SD D – – – SD SD D
albomicans F – – D – – – – – –
calloptera ornatipennis F – – D – – – – – –
funebris funebris F, M – – D – – – – – –
pseudoobscura pseudoobscura F SD D D – – – – – –
Tab.2  Summary of survival and toxin tolerance in mushroom-feeding Drosophila under different dietary conditions.
Fig.1  Four mechanisms that are hypothesized to contribute to the resistance to α-amanitin in the D. melanogaster Ama-KTT strain. α-Amanitin is shown as a red 8. Cuticular proteins block some of the α-amanitin from entering the cells (blockage). α-Amanitin that entered the cytoplasm is either sequestered in lipid particles, cleaved by peptidases, or detoxified by phase I and II detoxification enzymes, possibly followed by excretion. Figure adapted from Mitchell change to et al. (2014).
Fig.2  The TOR pathway may mediate α-amanitin resistance in the DGRP lines. α-Amanitin is shown as a red 8. The proteins Widerborst and Tequila are upstream regulators of TOR, influencing autophagy. TOR is a critical repressor of autophagy and Megalin-mediated endocytosis. Both the endocytic and autophagic catabolic processes end with the degradation and recycling of macromolecules in lysosomes. Megalin protein is hypothesized to sequester α-amanitin to the endosome, followed by the degradation of α-amanitin. Figure adapted from Mitchell change to et al. (2017).
1 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
https://doi.org/10.1111/j.1432-1033.2004.04025.x pmid: 15030474
2 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
https://doi.org/10.1046/j.1365-2540.2000.00729.x pmid: 11012721
3 Berger K J, Guss D A (2005a). Mycotoxins revisited: Part I. J Emerg Med, 28(1): 53–62
https://doi.org/10.1016/j.jemermed.2004.08.013 pmid: 15657006
4 Berger K J, Guss D A (2005b). Mycotoxins revisited: Part II. J Emerg Med, 28(2): 175–183
https://doi.org/10.1016/j.jemermed.2004.08.019 pmid: 15707814
5 Beutler J A, Der Marderosian A H (1981). Chemical variation in Amanita. J Nat Prod, 44(4): 422–431
https://doi.org/10.1021/np50016a005
6 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
pmid: 5892794
7 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
https://doi.org/10.1038/hdy.2013.124 pmid: 24326291
8 Bresinsky A, Besl H (1990) A color atlas of poisonous fungi: a handbook for pharmacists, doctors and biologists. Wolfe, Wurzburg, Germany, 295 pp.
9 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
https://doi.org/10.1111/evo.13062 pmid: 27596628
10 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
https://doi.org/10.1080/15563650701754763 pmid: 18163234
11 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
https://doi.org/10.3109/15563650.2011.635149 pmid: 22165864
12 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
https://doi.org/10.3109/15563650903438566 pmid: 20028214
13 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
https://doi.org/10.3109/15563650.2010.543906 pmid: 21192756
14 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
https://doi.org/10.1080/15563650802559632 pmid: 19065310
15 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
https://doi.org/10.3109/15563650.2012.746424 pmid: 23272763
16 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
pmid: 11721773
17 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
https://doi.org/10.1016/S0965-1748(96)00036-7 pmid: 8995791
18 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
https://doi.org/10.1073/pnas.251664698 pmid: 11805306
19 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
20 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
pmid: 1970571
21 Chang S T, Miles P G (2004) Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact. CRC Press, Boca Raton, FL, 451 pp.
22 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
pmid: 985999
23 Coyne J A, Orr H A (2004) Speciation. Sinauer Associates, Inc., Sunderland, Massachusetts, 545 pp.
24 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
https://doi.org/10.1016/j.ibmb.2007.02.008 pmid: 17456446
25 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
https://doi.org/10.1111/jeb.12158 pmid: 23663194
26 Diaz J H (2005). Syndromic diagnosis and management of confirmed mushroom poisonings. Crit Care Med, 33(2): 427–436
https://doi.org/10.1097/01.CCM.0000153531.69448.49 pmid: 15699849
27 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
https://doi.org/10.1038/sj.onc.1209782 pmid: 16819507
28 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
https://doi.org/10.1111/mec.12097 pmid: 23121224
29 Dyer K A, Burke C, Jaenike J (2011). Wolbachia-mediated persistence of mtDNA from a potentially extinct species. Mol Ecol, 20(13): 2805–2817
https://doi.org/10.1111/j.1365-294X.2011.05128.x pmid: 21595768
30 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
https://doi.org/10.1073/pnas.0605578104 pmid: 17242362
31 Dyer K A, Jaenike J (2005). Evolutionary dynamics of a spatially structured host-parasite association: Drosophila innubila and male-killing Wolbachia. Evolution, 59(7): 1518–1528
https://doi.org/10.1111/j.0014-3820.2005.tb01801.x pmid: 16153037
32 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
https://doi.org/10.1641/0006-3568(2000)050[0403:IDWEAC]2.0.CO;2
33 Enjalbert F, Gallion C, Jehl F, Monteil H (1993). Toxin content, phallotoxin and amatoxin composition of Amanita phalloides tissues. Toxicon, 31(6): 803–807
https://doi.org/10.1016/0041-0101(93)90386-W pmid: 8342178
34 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
https://doi.org/10.1081/CLT-120014646 pmid: 12475187
35 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
pmid: 24294010
36 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
https://doi.org/10.1016/j.jhep.2006.10.013 pmid: 17188393
37 Faulstich H (1980). Mushroom poisoning. Lancet, 2(8198): 794–795
https://doi.org/10.1016/S0140-6736(80)90400-6 pmid: 6107465
38 Faulstich H, Cochet-Meilhac M (1976). Amatoxins in edible mushrooms. FEBS Lett, 64(1): 73–75
https://doi.org/10.1016/0014-5793(76)80252-9 pmid: 1269766
39 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
https://doi.org/10.1111/j.1365-2583.2005.00532.x pmid: 15663776
40 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
https://doi.org/10.1111/j.1365-294X.2009.04380.x pmid: 19821901
41 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
https://doi.org/10.1016/j.jmgm.2014.05.002 pmid: 24879323
42 Gleixner E M, Canaud G, Hermle T, Guida M C, Kretz O, Helmstädter M, Huber T B, Eimer S, Terzi F, Simons M (2014). V-ATPase/mTOR signaling regulates megalin-mediated apical endocytosis. Cell Reports, 8(1): 10–19
https://doi.org/10.1016/j.celrep.2014.05.035 pmid: 24953654
43 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
https://doi.org/10.1016/0092-8674(79)90116-8 pmid: 117900
44 Grimaldi D (1985). Niche separation and competitive coexistence in mycophagous Drosophila (Diptera: Drosophilidae). Proc Entomol Soc Wash, 87: 498–511
45 Grimaldi D, Jaenike J (1984). Competition in natural populations of mycophagous Drosophila. Ecology, 65(4): 1113–1120
https://doi.org/10.2307/1938319
46 Hackman W, Meinander M (1979). Diptera feeding as larvae on macrofungi in Finland. Ann Zool Fenn, 16: 50–83
47 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
https://doi.org/10.1016/S0254-6299(15)30393-8
48 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
https://doi.org/10.1073/pnas.0707340104 pmid: 18025465
49 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
https://doi.org/10.1016/j.ympev.2009.02.022 pmid: 19285146
50 Heard S B, Hauser D L (1995). Key evolutionary innovations and their ecological mechanisms. Hist Biol, 10(2): 151–173
https://doi.org/10.1080/10292389509380518
51 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 M A, 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
https://doi.org/10.1101/gr.171546.113 pmid: 24714809
52 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
https://doi.org/10.1093/cz/zow005 pmid: 29491905
53 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
https://doi.org/10.1098/rspb.2005.3056 pmid: 16048766
54 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
https://doi.org/10.1371/journal.pone.0160051 pmid: 27462734
55 Jaenike J (1978a). Host selection by mycophagous Drosophila. Ecology, 59(6): 1286–1288
https://doi.org/10.2307/1938245
56 Jaenike J (1978b). Resource predictability and niche breadth in the Drosophila quinaria species group. Evolution, 32(3): 676–678
https://doi.org/10.1111/j.1558-5646.1978.tb04613.x pmid: 28567956
57 Jaenike J (1985a). Genetic and environmental determinants of food preference in Drosophila tripunctata. Evolution, 39(2): 362–369
https://doi.org/10.1111/j.1558-5646.1985.tb05673.x pmid: 28564210
58 Jaenike J (1985b). Parasite pressure and the evolution of amanitin tolerance in Drosophila. Evolution, 39(6): 1295–1301
https://doi.org/10.1111/j.1558-5646.1985.tb05695.x pmid: 28564265
59 Jaenike J (1986). Genetic complexity of host-selection behavior in Drosophila. Proc Natl Acad Sci USA, 83(7): 2148–2151
https://doi.org/10.1073/pnas.83.7.2148 pmid: 16593679
60 Jaenike J (1987). Genetics of oviposition-site preference in Drosophila tripunctata. Heredity (Edinb), 59(Pt 3): 363–369
https://doi.org/10.1038/hdy.1987.144 pmid: 3429258
61 Jaenike J (1989). Genetic population structure of Drosophila tripunctata: Patterns of varitation and covariation of traits affecting resource use. Evolution, 43(7): 1467–1482
pmid: 28564234
62 Jaenike J (1992). Mycophagous Drosophila and their nematode parasites. Am Nat, 139(5): 893–906
https://doi.org/10.1086/285365
63 Jaenike J, Dyer K A, Cornish C, Minhas M S (2006). Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol, 4(10): e325
https://doi.org/10.1371/journal.pbio.0040325 pmid: 17032063
64 Jaenike J, Grimaldi D (1983). Genetic variation for host preference within and among populations of Drosophila tripunctata. Evolution, 37(5): 1023–1033
https://doi.org/10.1111/j.1558-5646.1983.tb05630.x pmid: 28563549
65 Jaenike J, Grimaldi D A, Sluder A E, Greenleaf A L (1983). a-Amanitin tolerance in mycophagous Drosophila. Science, 221(4606): 165–167
https://doi.org/10.1126/science.221.4606.165 pmid: 17769215
66 Jaenike J, James A C (1991). Aggregation and the coexistence of mycophagous Drosophila. J Anim Ecol, 60(3): 913–928
https://doi.org/10.2307/5421
67 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
pmid: 18707451
68 Jaenike J, Selander R K (1979). Ecological generalism in Drosophila falleni: genetic evidence. Evolution, 33(2): 741–748
https://doi.org/10.1111/j.1558-5646.1979.tb04726.x pmid: 28563929
69 Kalač P (2009). Chemical composition and nutritional value of European species of wild growing mushrooms: a review. Food Chem, 113(1): 9–16
https://doi.org/10.1016/j.foodchem.2008.07.077
70 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
https://doi.org/10.1002/jsfa.5960 pmid: 23172575
71 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
https://doi.org/10.1371/journal.pone.0040296 pmid: 22768270
72 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
https://doi.org/10.1016/j.molcel.2008.04.023 pmid: 18538653
73 Karlson-Stiber C, Persson H (2003). Cytotoxic fungi--an overview. Toxicon, 42(4): 339–349
https://doi.org/10.1016/S0041-0101(03)00238-1 pmid: 14505933
74 Kaul T N (2002) Biology and conservation of mushrooms. Science Publishers, Inc., Enfield (NH), USA, 255 pp.
75 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
https://doi.org/10.1177/0748233713491809 pmid: 23719849
76 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
https://doi.org/10.1016/j.toxicon.2013.10.008 pmid: 24139877
77 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
https://doi.org/10.1073/pnas.1118589109 pmid: 23184999
78 Kim Y C, Guan K L (2015). mTOR: a pharmacologic target for autophagy regulation. J Clin Invest, 125(1): 25–32
https://doi.org/10.1172/JCI73939 pmid: 25654547
79 Kimura M T (1980). Evolution of food preferences in fungus-feeding Drosophila: an ecological study. Evolution, 34(5): 1009–1018
pmid: 28581130
80 Kimura M T, Toda M J (1989). Food preferences and nematode parasitism in mycophagous Drosophila. Ecol Res, 4(2): 209–218
https://doi.org/10.1007/BF02347153
81 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
https://doi.org/10.1038/srep25895 pmid: 27181033
82 Lacy R C (1984). Predictability, toxicity, and trophic niche breadth in fungus-feeding Drosophilidae (Diptera). Ecol Entomol, 9(1): 43–54
https://doi.org/10.1111/j.1365-2311.1984.tb00697.x
83 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
https://doi.org/10.1080/15563650600907165 pmid: 17015284
84 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
https://doi.org/10.1016/j.ibmb.2006.05.009 pmid: 16876710
85 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
https://doi.org/10.3109/15563659709001168 pmid: 9022655
86 Li C, Oberlies N H (2005). The most widely recognized mushroom: chemistry of the genus Amanita. Life Sci, 78(5): 532–538
https://doi.org/10.1016/j.lfs.2005.09.003 pmid: 16203016
87 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
https://doi.org/10.1126/science.170.3956.447 pmid: 4918258
88 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
https://doi.org/10.1016/0735-6757(95)90171-X pmid: 7662064
89 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
https://doi.org/10.1016/S0735-6757(96)90160-6 pmid: 8765118
90 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
https://doi.org/10.1016/S0735-6757(99)90254-1 pmid: 10496515
91 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
https://doi.org/10.1016/S0735-6757(98)90000-6 pmid: 9725964
92 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
https://doi.org/10.1053/ajem.2002.34955 pmid: 12216043
93 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
https://doi.org/10.1053/ajem.2000.9261 pmid: 10999572
94 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
https://doi.org/10.1053/ajem.2001.25272 pmid: 11555795
95 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
https://doi.org/10.1016/S0735-6757(97)90193-5 pmid: 9270389
96 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
https://doi.org/10.1038/nature14418 pmid: 25901683
97 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
https://doi.org/10.1038/nature10811 pmid: 22318601
98 Marciniak B, Łopaczyńska D, Ferenc T (2017). Evaluation of the genotoxicity of alpha-amanitin in mice bone marrow cells. Toxicon, 137: 1–6
https://doi.org/10.1016/j.toxicon.2017.07.005 pmid: 28688806
99 Mas A (2005). Mushrooms, amatoxins and the liver. J Hepatol, 42(2): 166–169
https://doi.org/10.1016/j.jhep.2004.12.003 pmid: 15664239
100 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
https://doi.org/10.1371/journal.pone.0173162 pmid: 28241077
101 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
https://doi.org/10.1371/journal.pone.0093489 pmid: 24695618
102 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
https://doi.org/10.1371/journal.pone.0127569 pmid: 25978397
103 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
https://doi.org/10.1093/jnci/djs140 pmid: 22457476
104 Morales-Hojas R, Vieira J (2012). Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. PLoS One, 7(11): e49552
https://doi.org/10.1371/journal.pone.0049552 pmid: 23152919
105 Moshnikova A, Moshnikova V, Andreev O A, Reshetnyak Y K (2013). Antiproliferative effect of pHLIP-amanitin. Biochemistry, 52(7): 1171–1178
https://doi.org/10.1021/bi301647y pmid: 23360641
106 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
https://doi.org/10.3109/15563650.2013.863906 pmid: 24359283
107 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
https://doi.org/10.3109/15563650.2014.987397 pmid: 25559822
108 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
https://doi.org/10.3390/molecules191219532 pmid: 25432007
109 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
https://doi.org/10.1111/j.0014-3820.2003.tb01546.x pmid: 12703944
110 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
https://doi.org/10.1046/j.1365-294X.2003.01721.x pmid: 12492892
111 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
https://doi.org/10.1139/g82-014 pmid: 6812932
112 Schluter D (2000) The ecology of adaptive radiation. Oxford University Press Inc., Oxford, New York.
113 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
https://doi.org/10.1111/j.1558-5646.1999.tb04529.x pmid: 28565520
114 Shorrocks B, Charlesworth P (1980). The distribution and abundance of the British fungal-breeding Drosophila. Ecol Entomol, 5(1): 61–78
https://doi.org/10.1111/j.1365-2311.1980.tb01124.x
115 Shorrocks B, Wood A M (1973). A preliminary note on the fungus feeding species of Drosophila. J Nat Hist, 7(5): 551–556
https://doi.org/10.1080/00222937300770441
116 Simpson G G (1953) The major features of evolution. Columbia University Press, New York, New York.
117 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
pmid: 28565683
118 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
https://doi.org/10.1098/rspb.2013.3333 pmid: 24648226
119 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
https://doi.org/10.1603/EN11136 pmid: 22217779
120 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
https://doi.org/10.3390/molecules21091201 pmid: 27617993
121 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
https://doi.org/10.1007/s10886-006-9228-3 pmid: 17195114
122 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
https://doi.org/10.1002/jps.2600550612 pmid: 5951044
123 Vetter J (1998). Toxins of Amanita phalloides. Toxicon, 36(1): 13–24
https://doi.org/10.1016/S0041-0101(97)00074-3 pmid: 9604278
124 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
https://doi.org/10.1002/bip.21416 pmid: 20564017
125 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
https://doi.org/10.1016/j.ajem.2004.06.001 pmid: 15490384
126 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
https://doi.org/10.1016/j.ajem.2005.05.001 pmid: 16140178
127 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
https://doi.org/10.1016/S0735-6757(03)00088-3 pmid: 14523881
128 Werner T (2017). The Drosophilids of a pristine old-growth northern hardwood forest. Great Lakes Entomol, 50: 68–78
129 Werner T, Jaenike J (2017) Drosophilids of the Midwest and Northeast. River Campus Libraries, University of Rochester, Rochester, NY, 256 pp.
130 Werren J H, Jaenike J (1995). Wolbachia and cytoplasmic incompatibility in mycophagous Drosophila and their relatives. Heredity (Edinb), 75(Pt 3): 320–326
https://doi.org/10.1038/hdy.1995.140 pmid: 7558891
131 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
https://doi.org/10.1126/science.159.3818.946 pmid: 4865716
132 Wieland T (1983). The toxic peptides from Amanita mushrooms. Int J Pept Protein Res, 22(3): 257–276
https://doi.org/10.1111/j.1399-3011.1983.tb02093.x pmid: 6354951
133 Wieland T (1986). Peptides of poisonous Amanita mushrooms. Springer-Verlag, New York, 256 pp.
134 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
https://doi.org/10.3109/10409237809149870 pmid: 363352
135 Yocum R R, Simons D M (1977). Amatoxins and phallotoxins in Amanita species of the Northeastern United States. Lloydia, 40: 178–190
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