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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| Published in: | BMC genomics Vol. 20; no. 1; pp. 413 - 17 |
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| Main Authors: | , |
| Format: | Journal Article |
| Language: | English |
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London
BioMed Central
22.05.2019
BioMed Central Ltd Springer Nature B.V BMC |
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| ISSN: | 1471-2164, 1471-2164 |
| Online Access: | Get full text |
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| Abstract | 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. |
|---|---|
| AbstractList | 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 [degrees]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 [degrees]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. Keywords: Thermal plasticity, Cold tolerance, Transcriptomics, Genes expression, Spotted wing drosophila 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 [degrees]C), and then compared transcriptomic responses of cold hardy versus cold susceptible phenotypes using RNA sequencing. 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. 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 [degrees]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. 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. 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. 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. 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. 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.BACKGROUNDInsects 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.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.RESULTSCold 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.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.CONCLUSIONSInvolvement 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. ("[en] 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.","[en] ","") 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. Abstract 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. |
| ArticleNumber | 413 |
| Audience | Academic |
| Author | Colinet, Hervé Enriquez, Thomas |
| Author_xml | – sequence: 1 givenname: Thomas orcidid: 0000-0003-3633-6043 surname: Enriquez fullname: Enriquez, Thomas email: thomas.enriquez.tours@gmail.com organization: Université de Rennes1, CNRS, ECOBIO – UMR 6553 – sequence: 2 givenname: Hervé surname: Colinet fullname: Colinet, Hervé organization: Université de Rennes1, CNRS, ECOBIO – UMR 6553 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31117947$$D View this record in MEDLINE/PubMed https://univ-rennes.hal.science/hal-02150230$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | The Author(s). 2019 COPYRIGHT 2019 BioMed Central Ltd. 2019. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Distributed under a Creative Commons Attribution 4.0 International License |
| Copyright_xml | – notice: The Author(s). 2019 – notice: COPYRIGHT 2019 BioMed Central Ltd. – notice: 2019. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Distributed under a Creative Commons Attribution 4.0 International License |
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| DOI | 10.1186/s12864-019-5745-7 |
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| Keywords | Genes expression Spotted wing drosophila Thermal plasticity Cold tolerance Transcriptomics |
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Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal... Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal conditions,... Background Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal... Background - Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal thermal... ("[en] BACKGROUND: Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal... Abstract Background Insects have the capacity to adjust their physiological mechanisms during their lifetime to promote cold tolerance and cope with sublethal... |
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| SubjectTerms | Acclimation Acclimatization Anatomie (cytologie, histologie, embryologie...) & physiologie Anatomy (cytology, histology, embryology...) & physiology Animal genetics Animal Genetics and Genomics Animals Annotations Bioengineering Bioinformatics Biological research Biomedical and Life Sciences Biotechnology Carbohydrate metabolism Carbohydrates Cold Cold acclimation Cold adaptation Cold Temperature Cold tolerance Coma Conditioning Drosophila Drosophila - classification Drosophila - genetics Drosophila - physiology Drosophila Proteins Drosophila Proteins - genetics Drosophila suzukii Eggs Entomologie & lutte antiravageur Entomology & pest control Environmental sciences & ecology Females Flies Fruits Gene expression Gene Expression Profiling Gene Expression Regulation Gene regulation Gene sequencing Genes Genes expression Genetic aspects Genetic research Genetics Genomes Genomics Homeostasis Insects Ion transport Life Sciences Metabolism Metabolites Microarrays Microbial Genetics and Genomics Multicellular invertebrate genomics Neurons Oogenesis Phenotypes Physiological aspects Physiology Plant Genetics and Genomics Proteomics Research Article Ribonucleic acid RNA RNA sequencing Sciences de l’environnement & écologie Sciences du vivant Spotted wing drosophila Temperature tolerance Thermal plasticity Thermotolerance Transcription Transcription (Genetics) Transcriptome Transcriptomics |
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| Title | Cold acclimation triggers major transcriptional changes in Drosophila suzukii |
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