Cold Acclimation Favors Metabolic Stability in Drosophila suzukii
The invasive fruit fly pest, Drosophila suzukii, is a chill susceptible species, yet it is capable of overwintering in rather cold climates, such as North America and North Europe, probably thanks to a high cold tolerance plasticity. Little is known about the mechanisms underlying cold tolerance acq...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-11-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2018.01506/full |
| _version_ | 1817993578359554048 |
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| author | Thomas Enriquez David Renault David Renault Maryvonne Charrier Hervé Colinet |
| author_facet | Thomas Enriquez David Renault David Renault Maryvonne Charrier Hervé Colinet |
| author_sort | Thomas Enriquez |
| collection | DOAJ |
| description | The invasive fruit fly pest, Drosophila suzukii, is a chill susceptible species, yet it is capable of overwintering in rather cold climates, such as North America and North Europe, probably thanks to a high cold tolerance plasticity. Little is known about the mechanisms underlying cold tolerance acquisition in D. suzukii. In this study, we compared the effect of different forms of cold acclimation (at juvenile or at adult stage) on subsequent cold tolerance. Combining developmental and adult cold acclimation resulted in a particularly high expression of cold tolerance. As found in other species, we expected that cold-acclimated flies would accumulate cryoprotectants and would be able to maintain metabolic homeostasis following cold stress. We used quantitative target GC-MS profiling to explore metabolic changes in four different phenotypes: control, cold acclimated during development or at adult stage or during both phases. We also performed a time-series GC-MS analysis to monitor metabolic homeostasis status during stress and recovery. The different thermal treatments resulted in highly distinct metabolic phenotypes. Flies submitted to both developmental and adult acclimation were characterized by accumulation of cryoprotectants (carbohydrates and amino acids), although concentrations changes remained of low magnitude. After cold shock, non-acclimated chill-susceptible phenotype displayed a symptomatic loss of metabolic homeostasis, correlated with erratic changes in the amino acids pool. On the other hand, the most cold-tolerant phenotype was able to maintain metabolic homeostasis after cold stress. These results indicate that cold tolerance acquisition of D. suzukii depends on physiological strategies similar to other drosophilids: moderate changes in cryoprotective substances and metabolic robustness. In addition, the results add to the body of evidence supporting that mechanisms underlying the different forms of acclimation are distinct. |
| first_indexed | 2024-04-14T01:41:47Z |
| format | Article |
| id | doaj.art-d45133480ee145658a513692523d6422 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-04-14T01:41:47Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-d45133480ee145658a513692523d64222022-12-22T02:19:43ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2018-11-01910.3389/fphys.2018.01506415192Cold Acclimation Favors Metabolic Stability in Drosophila suzukiiThomas Enriquez0David Renault1David Renault2Maryvonne Charrier3Hervé Colinet4ECOBIO – UMR 6553, Université de Rennes 1, CNRS, Rennes, FranceECOBIO – UMR 6553, Université de Rennes 1, CNRS, Rennes, FranceInstitut Universitaire de France, Paris, FranceECOBIO – UMR 6553, Université de Rennes 1, CNRS, Rennes, FranceECOBIO – UMR 6553, Université de Rennes 1, CNRS, Rennes, FranceThe invasive fruit fly pest, Drosophila suzukii, is a chill susceptible species, yet it is capable of overwintering in rather cold climates, such as North America and North Europe, probably thanks to a high cold tolerance plasticity. Little is known about the mechanisms underlying cold tolerance acquisition in D. suzukii. In this study, we compared the effect of different forms of cold acclimation (at juvenile or at adult stage) on subsequent cold tolerance. Combining developmental and adult cold acclimation resulted in a particularly high expression of cold tolerance. As found in other species, we expected that cold-acclimated flies would accumulate cryoprotectants and would be able to maintain metabolic homeostasis following cold stress. We used quantitative target GC-MS profiling to explore metabolic changes in four different phenotypes: control, cold acclimated during development or at adult stage or during both phases. We also performed a time-series GC-MS analysis to monitor metabolic homeostasis status during stress and recovery. The different thermal treatments resulted in highly distinct metabolic phenotypes. Flies submitted to both developmental and adult acclimation were characterized by accumulation of cryoprotectants (carbohydrates and amino acids), although concentrations changes remained of low magnitude. After cold shock, non-acclimated chill-susceptible phenotype displayed a symptomatic loss of metabolic homeostasis, correlated with erratic changes in the amino acids pool. On the other hand, the most cold-tolerant phenotype was able to maintain metabolic homeostasis after cold stress. These results indicate that cold tolerance acquisition of D. suzukii depends on physiological strategies similar to other drosophilids: moderate changes in cryoprotective substances and metabolic robustness. In addition, the results add to the body of evidence supporting that mechanisms underlying the different forms of acclimation are distinct.https://www.frontiersin.org/article/10.3389/fphys.2018.01506/fullspotted wing drosophilacold tolerancecold shockhomeostasisrecoverymetabolites |
| spellingShingle | Thomas Enriquez David Renault David Renault Maryvonne Charrier Hervé Colinet Cold Acclimation Favors Metabolic Stability in Drosophila suzukii Frontiers in Physiology spotted wing drosophila cold tolerance cold shock homeostasis recovery metabolites |
| title | Cold Acclimation Favors Metabolic Stability in Drosophila suzukii |
| title_full | Cold Acclimation Favors Metabolic Stability in Drosophila suzukii |
| title_fullStr | Cold Acclimation Favors Metabolic Stability in Drosophila suzukii |
| title_full_unstemmed | Cold Acclimation Favors Metabolic Stability in Drosophila suzukii |
| title_short | Cold Acclimation Favors Metabolic Stability in Drosophila suzukii |
| title_sort | cold acclimation favors metabolic stability in drosophila suzukii |
| topic | spotted wing drosophila cold tolerance cold shock homeostasis recovery metabolites |
| url | https://www.frontiersin.org/article/10.3389/fphys.2018.01506/full |
| work_keys_str_mv | AT thomasenriquez coldacclimationfavorsmetabolicstabilityindrosophilasuzukii AT davidrenault coldacclimationfavorsmetabolicstabilityindrosophilasuzukii AT davidrenault coldacclimationfavorsmetabolicstabilityindrosophilasuzukii AT maryvonnecharrier coldacclimationfavorsmetabolicstabilityindrosophilasuzukii AT hervecolinet coldacclimationfavorsmetabolicstabilityindrosophilasuzukii |