How herbivores coopt plant defenses: natural selection, specialization, and sequestration

Petschenka, Georg; Agrawal, Anurag A.

doi:10.1016/j.cois.2015.12.004

Cited by 147 publications

(143 citation statements)

References 51 publications

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“…These structures can form efficient protective mechanisms against hydrophilic or polar cardenolides such as ouabain that do not cross membranes passively (Figure 1) (Petschenka et al, 2013; Petschenka and Agrawal, 2016; Züst and Agrawal, 2016). In this way, polar cardenolides are to some extent prevented from reaching the nervous tissue where they could otherwise have adverse neurological effects (Armstrong et al, 2011; Ashmore et al, 2009; Schubiger et al, 1994; Xia et al, 1997, 1998).…”

Section: Introductionmentioning

confidence: 99%

Multidrug transporters and organic anion transporting polypeptides protect insects against the toxic effects of cardenolides

Groen

LaPlante

Alexandre

et al. 2017

Insect Biochemistry and Molecular Biology

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In the struggle against dietary toxins, insects are known to employ target site insensitivity, metabolic detoxification, and transporters that shunt away toxins. Specialized insects across six taxonomic orders feeding on cardenolide-containing plants have convergently evolved target site insensitivity via specific amino acid substitutions in the Na/K-ATPase. Nonetheless, in vitro pharmacological experiments have suggested a role for multidrug transporters (Mdrs) and organic anion transporting polypeptides (Oatps), which may provide a basal level of protection in both specialized and non-adapted insects. Because the genes coding for these proteins are evolutionarily conserved and in vivo genetic evidence in support of this hypothesis is lacking, here we used wildtype and mutant Drosophila melanogaster (Drosophila) in capillary feeder (CAFE) assays to quantify toxicity of three chemically diverse, medically relevant cardenolides. We examined multiple components of fitness, including mortality, longevity, and LD50, and found that, while the three cardenolides each stimulated feeding (i.e., no deterrence to the toxin), all decreased lifespan, with the most apolar cardenolide having the lowest LD50 value. Flies showed a clear non-monotonic dose response and experienced high levels of toxicity at the cardenolide concentration found in plants. At this concentration, both Mdr and Oatp knockout mutant flies died more rapidly than wildtype flies, and the mutants also experienced more adverse neurological effects on high-cardenolide-level diets. Our study further establishes Drosophila as a model for the study of cardenolide pharmacology and solidifies support for the hypothesis that multidrug and organic anion transporters are key players in insect protection against dietary cardenolides.

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Section: Introductionmentioning

confidence: 99%

Multidrug transporters and organic anion transporting polypeptides protect insects against the toxic effects of cardenolides

Groen

LaPlante

Alexandre

et al. 2017

Insect Biochemistry and Molecular Biology

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“…Insects use iridoids frequently as chemical stimuli for communication or defense [41][42][43][44][45][46][47]. Although many insects profit from the sequestration of iridoid glucosides from their host plants [16,[48][49][50], others, such as stick insects [51], rove beetles [40], or leaf beetles [52][53][54][55][56] are able to produce iridoids de novo.…”

Section: Introductionmentioning

confidence: 99%

Deciphering the route to cyclic monoterpenes in Chrysomelina leaf beetles: source of new biocatalysts for industrial application?

Burse

Boland

2017

Zeitschrift Für Naturforschung C

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Abstract:The drastic growth of the population on our planet requires the efficient and sustainable use of our natural resources. Enzymes are indispensable tools for a wide range of industries producing food, pharmaceuticals, pesticides, or biofuels. Because insects constitute one of the most species-rich classes of organisms colonizing almost every ecological niche on earth, they have developed extraordinary metabolic abilities to survive in various and sometimes extreme habitats. Despite this metabolic diversity, insect enzymes have only recently generated interest in industrial applications because only a few metabolic pathways have been sufficiently characterized. Here, we address the biosynthetic route to iridoids (cyclic monoterpenes), a group of secondary metabolites used by some members of the leaf beetle subtribe Chrysomelina as defensive compounds against their enemies. The ability to produce iridoids de novo has also convergently evolved in plants. From plant sources, numerous pharmacologically relevant structures have already been described. In addition, in plants, iridoids serve as building blocks for monoterpenoid indole alkaloids with broad therapeutic applications. As the commercial synthesis of iridoidbased drugs often relies on a semisynthetic approach involving biocatalysts, the discovery of enzymes from the insect iridoid route can account for a valuable resource and economic alternative to the previously used enzymes from the metabolism of plants. Hence, this review illustrates the recent discoveries made on the steps of the iridoid pathway in Chrysomelina leaf beetles. The findings are also placed in the context of the studied counterparts in plants and are further discussed regarding their use in technological approaches.

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“…Plant-insect interactions have evolved so intricately and have enabled insects to adopt a generalist or specialist feeding behaviour (Mello and Silva-Filho 2002). This interaction is also greatly influenced by the defence mechanisms developed by their host plants (Petschenka and Agrawal 2016). Specialists have developed highly efficient mechanisms to counteract the effects of chemical toxins while generalists compromise certain aspects of their lifecycle to overcome the defence mechanisms of plants (Mello and Silva-Filho 2002;Price et al 1980).…”

Section: Plant Herbivory and Determining Food Plants Of Insectsmentioning

confidence: 99%

Elucidating food plants of the aggregative, synchronously flashing Southeast Asian firefly, Pteroptyx tener Olivier (Coleoptera, Lampyridae)

Cheng¹,

Chan²,

Ishak³

et al. 2017

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The aggregative, synchronously flashing firefly, Pteroptyx tener congregates on a nightly basis on Berembang trees (Sonneratia caseolaris) growing along the lower reaches of the Selangor River (West Malaysia). Every night, the males and females of this species engage one another in a pre-mating ritual of flash communication. Little is known of the dietary requirements of the adults of P. tener apart from suggestions that these beetles feed on the nectar and sap of mangrove trees. The drastic reduction in their numbers in recent years has sparked an urgency to understand their dietary needs. Here, we report on a series of probing experiments where we sequenced and analysed DNA fragments obtained from the gut contents of adult P. tener specimens. We detected coding and non-coding chloroplast DNA (cpDNA) gene sequences in the gut DNA extracts of P. tener. One DNA sequence was in reasonably good condition to allow us to match it to the cpDNA sequence of a Malvacean, that is, Heritiera littoralis, a common inhabitant of estuarine habitats. We also detected the DNA sequences of plants (cultivated and natural) that may have come from hamlets or isolated freshwater swamps located further inland. The findings reported here provide early indication that P. tener may be able to travel further inland to search for their hosts. Future research should focus on visually confirming if P. tener feeds on H. littoralis and obtaining a more complete reference DNA database of plants in the firefly habitat.

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How herbivores coopt plant defenses: natural selection, specialization, and sequestration

Cited by 147 publications

References 51 publications

Multidrug transporters and organic anion transporting polypeptides protect insects against the toxic effects of cardenolides

Multidrug transporters and organic anion transporting polypeptides protect insects against the toxic effects of cardenolides

Deciphering the route to cyclic monoterpenes in Chrysomelina leaf beetles: source of new biocatalysts for industrial application?

Elucidating food plants of the aggregative, synchronously flashing Southeast Asian firefly, Pteroptyx tener Olivier (Coleoptera, Lampyridae)

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