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      Multiple stressors produce differential transcriptomic patterns in a stream-dwelling salamander

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          Abstract

          Background

          Global biodiversity is decreasing at an alarming rate and amphibians are at the forefront of this crisis. Understanding the factors that negatively impact amphibian populations and effectively monitoring their health are fundamental to addressing this epidemic. Plasma glucocorticoids are often used to assess stress in amphibians and other vertebrates, but these hormones can be extremely dynamic and impractical to quantify in small organisms. Transcriptomic responses to stress hormones in amphibians have been largely limited to laboratory models, and there have been few studies on vertebrates that have evaluated the impact of multiple stressors on patterns of gene expression. Here we examined the gene expression patterns in tail tissues of stream-dwelling salamanders ( Eurycea tynerensis) chronically exposed to the stress hormone corticosterone under different temperature regimes.

          Results

          We found unique transcriptional signatures for chronic corticosterone exposure that were independent of temperature variation. Several of the corticosterone responsive genes are known to be involved in immune system response ( LY-6E), oxidative stress ( GSTM2 and TRX), and tissue repair ( A2M and FX) . We also found many genes to be influenced by temperature ( CIRBP, HSC71, HSP40, HSP90, HSP70, ZNF593). Furthermore, the expression patterns of some genes ( GSTM2, LY-6E, UMOD, ZNF593, CIRBP, HSP90) show interactive effects of temperature and corticosterone exposure, compared to each treatment alone. Through a series of experiments we also showed that stressor induced patterns of expression were largely consistent across ages, life cycle modes, and tissue regeneration.

          Conclusions

          Outside of thermal stressors, the application of transcriptomes to monitor the health of non-human vertebrate systems has been vastly underinvestigated. Our study suggests that transcriptomic patterns harbor stressor specific signatures that can be highly informative for monitoring the diverse stressors of amphibian populations.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-5814-y) contains supplementary material, which is available to authorized users.

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          Most cited references77

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          edgeR: a Bioconductor package for differential expression analysis of digital gene expression data

          Summary: It is expected that emerging digital gene expression (DGE) technologies will overtake microarray technologies in the near future for many functional genomics applications. One of the fundamental data analysis tasks, especially for gene expression studies, involves determining whether there is evidence that counts for a transcript or exon are significantly different across experimental conditions. edgeR is a Bioconductor software package for examining differential expression of replicated count data. An overdispersed Poisson model is used to account for both biological and technical variability. Empirical Bayes methods are used to moderate the degree of overdispersion across transcripts, improving the reliability of inference. The methodology can be used even with the most minimal levels of replication, provided at least one phenotype or experimental condition is replicated. The software may have other applications beyond sequencing data, such as proteome peptide count data. Availability: The package is freely available under the LGPL licence from the Bioconductor web site (http://bioconductor.org). Contact: mrobinson@wehi.edu.au
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            The future of biodiversity.

            Recent extinction rates are 100 to 1000 times their pre-human levels in well-known, but taxonomically diverse groups from widely different environments. If all species currently deemed "threatened" become extinct in the next century, then future extinction rates will be 10 times recent rates. Some threatened species will survive the century, but many species not now threatened will succumb. Regions rich in species found only within them (endemics) dominate the global patterns of extinction. Although new technology provides details of habitat losses, estimates of future extinctions are hampered by our limited knowledge of which areas are rich in endemics.
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              The heat-shock response.

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                Author and article information

                Contributors
                tim.clay@nicholls.edu
                Michael.Steffen@unh.edu
                michael.treglia@tnc.org
                carolyndiane100@gmail.com
                ana-trujano@utulsa.edu
                ron-bonett@utulsa.edu
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                11 June 2019
                11 June 2019
                2019
                : 20
                : 482
                Affiliations
                [1 ]ISNI 0000 0001 2160 264X, GRID grid.267360.6, Department of Biological Science, , University of Tulsa, ; Tulsa, OK 74104 USA
                [2 ]ISNI 0000 0000 9473 1066, GRID grid.260957.f, Present Address: Department of Biological Sciences, Nicholls State University, ; Thibodaux, LA 70310 USA
                [3 ]ISNI 0000 0001 2192 7145, GRID grid.167436.1, Present Address: Department of Biological Sciences, , University of New Hampshire, ; Durham, NH 03824 USA
                [4 ]Present Address: The Nature Conservancy, New York, NY 10001 USA
                Author information
                http://orcid.org/0000-0002-2708-3446
                Article
                5814
                10.1186/s12864-019-5814-y
                6560913
                31185901
                68a2a5c5-1a4e-4498-8a2c-123f8f1349a9
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 26 July 2018
                : 20 May 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IIA-1301789
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                biomarkers,transcriptome,stress,salamander
                Genetics
                biomarkers, transcriptome, stress, salamander

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