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

Chialvo, Clare H. Scott; Werner, Thomas

doi:10.1007/s11515-018-1487-1

Cited by 17 publications

(17 citation statements)

References 117 publications

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“…For example, D. innubila is infected with a male‐killing, maternally transmitted pathogen, called Wolbachia which has been extensively studied (Dyer, 2004; Dyer & Jaenike, 2005; Dyer et al., 2005; Jaenike et al., 2003). D. innubila is also frequently exposed to a highly virulent DNA virus (Unckless, 2011), as well as toxic mushrooms (Scott Chialvo & Werner, 2018). Given these environmental and pathogenic factors, we expect to identify recent signatures of evolution in the D. innubila genome on establishment in the Sky Islands, as well as signatures of a recent population migration.…”

Section: Introductionmentioning

confidence: 99%

Adaptation, ancestral variation and gene flow in a ‘Sky Island’ Drosophila species

Hill

Unckless

2020

Molecular Ecology

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Section: Introductionmentioning

confidence: 99%

Adaptation, ancestral variation and gene flow in a ‘Sky Island’ Drosophila species

Hill

Unckless

2020

Molecular Ecology

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“…Several species of mushrooms of the genus Amanita contain significant amounts of cyclopeptide toxins in their tissues (Li & Oberlies, 2005). There are 17 known species of mycophagous Drosophila that use mushrooms that contain cyclopeptides toxins as developmental hosts (Scott‐Chialvo & Werner, 2018). No clear physiological mechanism for this tolerance has yet been identified, although it is clear that it is not due to target site insensitivity or behavioral avoidance (Jaenike et al., 1983).…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, many animals utilize their natural microbiota to detoxify harmful compounds they encounter in their environment (Ceja‐Navarro et al., 2015; Hammerbacher et al., 2013; Kohl, Weiss, Cox, Dale, & Dearing, 2014). Many species of Drosophila are generalists on Basidiomycota mushrooms, where they can spend their entire life cycle (Hackman & Meinander, 1979; Jaenike, 1978a, 1978b; Kimura & Toda, 1989; Lacy, 1984; Scott‐Chialvo & Werner, 2018; Shorrocks & Charlesworth, 1980). These insects are also among the only known eukaryotes to tolerate the amatoxins found in many of the mushrooms of this group (Jaenike, 1985; Jaenike, Grimaldi, Sluder, & Greenleaf, 1983; Scott‐Chialvo & Werner, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Many species of Drosophila are generalists on Basidiomycota mushrooms, where they can spend their entire life cycle (Hackman & Meinander, 1979; Jaenike, 1978a, 1978b; Kimura & Toda, 1989; Lacy, 1984; Scott‐Chialvo & Werner, 2018; Shorrocks & Charlesworth, 1980). These insects are also among the only known eukaryotes to tolerate the amatoxins found in many of the mushrooms of this group (Jaenike, 1985; Jaenike, Grimaldi, Sluder, & Greenleaf, 1983; Scott‐Chialvo & Werner, 2018). Chief among these toxins is α‐amanitin, which acts by binding to primarily RNA polymerase II (RNAP II) and inhibiting transcription (Lindell, Weinberg, Morris, Roeder, & Rutter, 1970).…”

Section: Introductionmentioning

confidence: 99%

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Effect of gut microbiota on α‐amanitin tolerance in Drosophila tripunctata

Griffin

Reed

2020

Ecology and Evolution

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The bacterial gut microbiota of many animals is known to be important for many physiological functions including detoxification. The selective pressures imposed on insects by exposure to toxins may also be selective pressures on their symbiotic bacteria, who thus may contribute to the mechanism of toxin tolerance for the insect. Amatoxins are a class of cyclopeptide mushroom toxins that primarily act by binding to RNA polymerase II and inhibiting transcription. Several species of mycophagous Drosophila are tolerant to amatoxins found in mushrooms of the genus Amanita, despite these toxins being lethal to most other known eukaryotes. These species can tolerate amatoxins in natural concentrations to utilize toxic mushrooms as larval hosts, but the mechanism by which these species are tolerant remains unknown. Previous data have shown that a local population of D. tripunctata exhibits significant genetic variation in toxin tolerance. This study assesses the potential role of the microbiome in α‐amanitin tolerance in six wild‐derived strains of Drosophila tripunctata. Normal and antibiotic‐treated samples of six strains were reared on diets with and without α‐amanitin, and then scored for survival from the larval stage to adulthood and for development time to pupation. Our results show that a substantial reduction in bacterial load does not influence toxin tolerance in this system, while confirming genotype and toxin‐specific effects on survival are independent of the microbiome composition. Thus, we conclude that this adaptation to exploit toxic mushrooms as a host is likely intrinsic to the fly's genome and not a property of their microbiome.

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“…While A. phalloides and other mushrooms that contain cyclopeptides are lethal to many eukaryotic organisms, at least 17 mushroom‐feeding Drosophila species (flies) use these toxic mushrooms and other nontoxic species as developmental hosts (Jaenike & James, 1991; Lacy, 1984). Very little is known about cyclopeptide tolerance in these fly species (reviewed in Scott Chialvo & Werner, 2018). Furthermore, studies examining this adaptation focused exclusively on the effect of α‐amanitin (Jaenike, Grimaldi, Sluder, & Greenleaf, 1983; Spicer & Jaenike, 1996; Stump, Jablonski, Bouton, & Wilder, 2011).…”

Section: Introductionmentioning

confidence: 99%

Exhaustive extraction of cyclopeptides from Amanita phalloides: Guidelines for working with complex mixtures of secondary metabolites

Chialvo

Griffin

Reed

et al. 2020

Ecology and Evolution

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Understanding plant‐insect interactions is an active area of research in both ecology and evolution. Much attention has been focused on the impact of secondary metabolites in the host plant or fungi on these interactions. Plants and fungi contain a variety of biologically active compounds, and the secondary metabolite profile can vary significantly between individual samples. However, many experiments characterize the biological effects of only a single secondary metabolite or a subset of these compounds. Here, we develop an exhaustive extraction protocol using an accelerated solvent extraction protocol to recover the complete suite of cyclopeptides and other secondary metabolites found in Amanita phalloides (death cap mushrooms) and compare its efficacy to the “Classic” extraction method used in earlier works. We demonstrate that our extraction protocol recovers the full suite of cyclopeptides and other secondary metabolites in A. phalloides unlike the “Classic” method that favors polar cyclopeptides. Based on these findings, we provide recommendations for how to optimize protocols to ensure exhaustive extracts and also the best practices when using natural extracts in ecological experiments.

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

Cited by 17 publications

References 117 publications

Adaptation, ancestral variation and gene flow in a ‘Sky Island’ Drosophila species

Adaptation, ancestral variation and gene flow in a ‘Sky Island’ Drosophila species

Effect of gut microbiota on α‐amanitin tolerance in Drosophila tripunctata

Exhaustive extraction of cyclopeptides from Amanita phalloides: Guidelines for working with complex mixtures of secondary metabolites

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