Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog

In the anuran family Dendrobatidae, aposematic species obtain their toxic or unpalatable alkaloids from dietary sources, a process known as sequestering. To understand how toxicity evolved in this family, it is paramount to elucidate the pathways of alkaloid processing (absorption, metabolism, and s...

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Main Authors: Eugenia Sanchez, Ariel Rodríguez, Jose H. Grau, Stefan Lötters, Sven Künzel, Ralph A. Saporito, Eva Ringler, Stefan Schulz, Katharina C. Wollenberg Valero, Miguel Vences
Format: Article
Language:English
Published: MDPI AG 2019-09-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/10/10/733
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spelling doaj-eab35f1c8d2c4704a991789e0746b6692020-11-25T01:22:45ZengMDPI AGGenes2073-44252019-09-01101073310.3390/genes10100733genes10100733Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison FrogEugenia Sanchez0Ariel Rodríguez1Jose H. Grau2Stefan Lötters3Sven Künzel4Ralph A. Saporito5Eva Ringler6Stefan Schulz7Katharina C. Wollenberg Valero8Miguel Vences9Zoological Institute, Technische Universität Braunschweig, 38106 Braunschweig, GermanyInstitut fur Zoologie, Tierärztliche Hochschule Hannover, 30559 Hannover, GermanyMuseum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, 10115 Berlin, GermanyBiogeography Department, Trier University, 54296 Trier, GermanyDepartment of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, 24306 Plön, GermanyDepartment of Biology, John Carroll University, University Heights, OH 44118, USAMesserli Research Institute, University of Veterinary Medicine Vienna, Medical University of Vienna, and University of Vienna, A-1210 Vienna, AustriaInstitute of Organic Chemistry, Technische Universität Braunschweig, 38106 Braunschweig, GermanyDepartment of Biological and Marine Sciences, University of Hull, Kingston-Upon Hull 01482, UKZoological Institute, Technische Universität Braunschweig, 38106 Braunschweig, GermanyIn the anuran family Dendrobatidae, aposematic species obtain their toxic or unpalatable alkaloids from dietary sources, a process known as sequestering. To understand how toxicity evolved in this family, it is paramount to elucidate the pathways of alkaloid processing (absorption, metabolism, and sequestering). Here, we used an exploratory skin gene expression experiment in which captive-bred dendrobatids were fed alkaloids. Most of these experiments were performed with <i>Dendrobates tinctorius</i>, but some trials were performed with <i>D. auratus</i>, <i>D. leucomelas</i> and <i>Allobates femoralis</i> to explore whether other dendrobatids would show similar patterns of gene expression. We found a consistent pattern of up-regulation of genes related to muscle and mitochondrial processes, probably due to the lack of mutations related to alkaloid resistance in these species. Considering conserved pathways of drug metabolism in vertebrates, we hypothesize alkaloid degradation is a physiological mechanism of resistance, which was evidenced by a strong upregulation of the immune system in <i>D. tinctorius</i>, and of complement C2 across the four species sampled. Probably related to this strong immune response, we found several skin keratins downregulated, which might be linked to a reduction of the cornified layer of the epidermis. Although not conclusive, our results offer candidate genes and testable hypotheses to elucidate alkaloid processing in poison frogs.https://www.mdpi.com/2073-4425/10/10/733DendrobatidaeAromobatidae<i>Dendrobates</i>Allobatesepibatidinegene expressionfeeding experimentimmune systemresistance
collection DOAJ
language English
format Article
sources DOAJ
author Eugenia Sanchez
Ariel Rodríguez
Jose H. Grau
Stefan Lötters
Sven Künzel
Ralph A. Saporito
Eva Ringler
Stefan Schulz
Katharina C. Wollenberg Valero
Miguel Vences
spellingShingle Eugenia Sanchez
Ariel Rodríguez
Jose H. Grau
Stefan Lötters
Sven Künzel
Ralph A. Saporito
Eva Ringler
Stefan Schulz
Katharina C. Wollenberg Valero
Miguel Vences
Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
Genes
Dendrobatidae
Aromobatidae
<i>Dendrobates</i>
Allobates
epibatidine
gene expression
feeding experiment
immune system
resistance
author_facet Eugenia Sanchez
Ariel Rodríguez
Jose H. Grau
Stefan Lötters
Sven Künzel
Ralph A. Saporito
Eva Ringler
Stefan Schulz
Katharina C. Wollenberg Valero
Miguel Vences
author_sort Eugenia Sanchez
title Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
title_short Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
title_full Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
title_fullStr Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
title_full_unstemmed Transcriptomic Signatures of Experimental Alkaloid Consumption in a Poison Frog
title_sort transcriptomic signatures of experimental alkaloid consumption in a poison frog
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2019-09-01
description In the anuran family Dendrobatidae, aposematic species obtain their toxic or unpalatable alkaloids from dietary sources, a process known as sequestering. To understand how toxicity evolved in this family, it is paramount to elucidate the pathways of alkaloid processing (absorption, metabolism, and sequestering). Here, we used an exploratory skin gene expression experiment in which captive-bred dendrobatids were fed alkaloids. Most of these experiments were performed with <i>Dendrobates tinctorius</i>, but some trials were performed with <i>D. auratus</i>, <i>D. leucomelas</i> and <i>Allobates femoralis</i> to explore whether other dendrobatids would show similar patterns of gene expression. We found a consistent pattern of up-regulation of genes related to muscle and mitochondrial processes, probably due to the lack of mutations related to alkaloid resistance in these species. Considering conserved pathways of drug metabolism in vertebrates, we hypothesize alkaloid degradation is a physiological mechanism of resistance, which was evidenced by a strong upregulation of the immune system in <i>D. tinctorius</i>, and of complement C2 across the four species sampled. Probably related to this strong immune response, we found several skin keratins downregulated, which might be linked to a reduction of the cornified layer of the epidermis. Although not conclusive, our results offer candidate genes and testable hypotheses to elucidate alkaloid processing in poison frogs.
topic Dendrobatidae
Aromobatidae
<i>Dendrobates</i>
Allobates
epibatidine
gene expression
feeding experiment
immune system
resistance
url https://www.mdpi.com/2073-4425/10/10/733
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