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Cold acclimation triggers major transcriptional changes in Drosophila suzukii

BACKGROUND: Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal conditions, a phenomenon referred to as thermal acclimation. The spotted wing drosophila, Drosophila suzukii, is an invasive fruit pest that,...

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Autores principales: Enriquez, Thomas, Colinet, Hervé
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6532241/
https://www.ncbi.nlm.nih.gov/pubmed/31117947
http://dx.doi.org/10.1186/s12864-019-5745-7
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author Enriquez, Thomas
Colinet, Hervé
author_facet Enriquez, Thomas
Colinet, Hervé
author_sort Enriquez, Thomas
collection PubMed
description BACKGROUND: Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal conditions, a phenomenon referred to as thermal acclimation. The spotted wing drosophila, Drosophila suzukii, is an invasive fruit pest that, like many other species, enhances its thermotolerance in response to thermal acclimation. However, little is known about the underlying mechanisms of this plastic response. Here, we promoted flies’ cold tolerance by gradually increasing acclimation duration (i.e. pre-exposure from 2 h to 9 days at 10 °C), and then compared transcriptomic responses of cold hardy versus cold susceptible phenotypes using RNA sequencing. RESULTS: Cold tolerance of D. suzukii increased with acclimation duration; the longer the acclimation, the higher the cold tolerance. Cold-tolerant flies that were acclimated for 9 days were selected for transcriptomic analyses. RNA sequencing revealed a total of 2908 differentially expressed genes: 1583 were up- and 1325 were downregulated in cold acclimated flies. Functional annotation revealed many enriched GO-terms among which ionic transport across membranes and signaling were highly represented in acclimated flies. Neuronal activity and carbohydrate metabolism were also enriched GO-terms in acclimated flies. Results also revealed many GO-terms related to oogenesis which were underrepresented in acclimated flies. CONCLUSIONS: Involvement of a large cluster of genes related to ion transport in cold acclimated flies suggests adjustments in the capacity to maintain ion and water homeostasis. These processes are key mechanisms underlying cold tolerance in insects. Down regulation of genes related to oogenesis in cold acclimated females likely reflects that females were conditioned at 10 °C, a temperature that prevents oogenesis. Overall, these results help to understand the molecular underpinnings of cold tolerance acquisition in D. suzukii. These data are of importance considering that the invasive success of D. suzukii in diverse climatic regions relates to its high thermal plasticity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5745-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-65322412019-05-29 Cold acclimation triggers major transcriptional changes in Drosophila suzukii Enriquez, Thomas Colinet, Hervé BMC Genomics Research Article BACKGROUND: Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal conditions, a phenomenon referred to as thermal acclimation. The spotted wing drosophila, Drosophila suzukii, is an invasive fruit pest that, like many other species, enhances its thermotolerance in response to thermal acclimation. However, little is known about the underlying mechanisms of this plastic response. Here, we promoted flies’ cold tolerance by gradually increasing acclimation duration (i.e. pre-exposure from 2 h to 9 days at 10 °C), and then compared transcriptomic responses of cold hardy versus cold susceptible phenotypes using RNA sequencing. RESULTS: Cold tolerance of D. suzukii increased with acclimation duration; the longer the acclimation, the higher the cold tolerance. Cold-tolerant flies that were acclimated for 9 days were selected for transcriptomic analyses. RNA sequencing revealed a total of 2908 differentially expressed genes: 1583 were up- and 1325 were downregulated in cold acclimated flies. Functional annotation revealed many enriched GO-terms among which ionic transport across membranes and signaling were highly represented in acclimated flies. Neuronal activity and carbohydrate metabolism were also enriched GO-terms in acclimated flies. Results also revealed many GO-terms related to oogenesis which were underrepresented in acclimated flies. CONCLUSIONS: Involvement of a large cluster of genes related to ion transport in cold acclimated flies suggests adjustments in the capacity to maintain ion and water homeostasis. These processes are key mechanisms underlying cold tolerance in insects. Down regulation of genes related to oogenesis in cold acclimated females likely reflects that females were conditioned at 10 °C, a temperature that prevents oogenesis. Overall, these results help to understand the molecular underpinnings of cold tolerance acquisition in D. suzukii. These data are of importance considering that the invasive success of D. suzukii in diverse climatic regions relates to its high thermal plasticity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5745-7) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-22 /pmc/articles/PMC6532241/ /pubmed/31117947 http://dx.doi.org/10.1186/s12864-019-5745-7 Text en © 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.
spellingShingle Research Article
Enriquez, Thomas
Colinet, Hervé
Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title_full Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title_fullStr Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title_full_unstemmed Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title_short Cold acclimation triggers major transcriptional changes in Drosophila suzukii
title_sort cold acclimation triggers major transcriptional changes in drosophila suzukii
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6532241/
https://www.ncbi.nlm.nih.gov/pubmed/31117947
http://dx.doi.org/10.1186/s12864-019-5745-7
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