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      Long-Term Cold Acclimation Extends Survival Time at 0°C and Modifies the Metabolomic Profiles of the Larvae of the Fruit Fly Drosophila melanogaster

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          Abstract

          Background

          Drosophila melanogaster is a chill-susceptible insect. Previous studies on this fly focused on acute direct chilling injury during cold shock and showed that lower lethal temperature (LLT, approximately −5°C) exhibits relatively low plasticity and that acclimations, both rapid cold hardening (RCH) and long-term cold acclimation, shift the LLT by only a few degrees at the maximum.

          Principal Findings

          We found that long-term cold acclimation considerably improved cold tolerance in fully grown third-instar larvae of D. melanogaster. A comparison of the larvae acclimated at constant 25°C with those acclimated at constant 15°C followed by constant 6°C for 2 d (15°C→6°C) showed that long-term cold acclimation extended the lethal time for 50% of the population (Lt 50) during exposure to constant 0°C as much as 630-fold (from 0.137 h to 86.658 h). Such marked physiological plasticity in Lt 50 (in contrast to LLT) suggested that chronic indirect chilling injury at 0°C differs from that caused by cold shock. Long-term cold acclimation modified the metabolomic profiles of the larvae. Accumulations of proline (up to 17.7 mM) and trehalose (up to 36.5 mM) were the two most prominent responses. In addition, restructuring of the glycerophospholipid composition of biological membranes was observed. The relative proportion of glycerophosphoethanolamines (especially those with linoleic acid at the sn-2 position) increased at the expense of glycerophosphocholines.

          Conclusion

          Third-instar larvae of D. melanogaster improved their cold tolerance in response to long-term cold acclimation and showed metabolic potential for the accumulation of proline and trehalose and for membrane restructuring.

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          Most cited references102

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          Mechanisms of plant desiccation tolerance.

          Anhydrobiosis ("life without water") is the remarkable ability of certain organisms to survive almost total dehydration. It requires a coordinated series of events during dehydration that are associated with preventing oxidative damage and maintaining the native structure of macromolecules and membranes. The preferential hydration of macromolecules is essential when there is still bulk water present, but replacement by sugars becomes important upon further drying. Recent advances in our understanding of the mechanism of anhydrobiosis include the downregulation of metabolism, dehydration-induced partitioning of amphiphilic compounds into membranes and immobilization of the cytoplasm in a stable multicomponent glassy matrix.
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            Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?

            J R Hazel (1995)
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              Living with water stress: evolution of osmolyte systems.

              Striking convergent evolution is found in the properties of the organic osmotic solute (osmolyte) systems observed in bacteria, plants, and animals. Polyhydric alcohols, free amino acids and their derivatives, and combinations of urea and methylamines are the three types of osmolyte systems found in all water-stressed organisms except the halobacteria. The selective advantages of the organic osmolyte systems are, first, a compatibility with macromolecular structure and function at high or variable (or both) osmolyte concentrations, and, second, greatly reduced needs for modifying proteins to function in concentrated intracellular solutions. Osmolyte compatibility is proposed to result from the absence of osmolyte interactions with substrates and cofactors, and the nonperturbing or favorable effects of osmolytes on macromolecular-solvent interactions.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                21 September 2011
                : 6
                : 9
                : e25025
                Affiliations
                [1 ]Institute of Entomology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
                [2 ]Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic
                University of Dayton, United States of America
                Author notes

                Conceived and designed the experiments: VK. Performed the experiments: VK JK JR HZ JC AT. Analyzed the data: VK HZ AT PS. Contributed reagents/materials/analysis tools: PS. Wrote the paper: VK.

                Article
                PONE-D-11-11907
                10.1371/journal.pone.0025025
                3177886
                21957472
                dbb45736-b752-48be-bfb2-c5d2c62905f7
                Kostal et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 27 June 2011
                : 22 August 2011
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Integrative Physiology
                Biochemistry
                Metabolism
                Carbohydrate Metabolism
                Metabolic Pathways
                Cryobiology
                Model Organisms
                Animal Models
                Drosophila Melanogaster
                Molecular Cell Biology
                Cellular Stress Responses
                Chemistry
                Organic Chemistry
                Organic Acids
                Amino Acids

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                Uncategorized

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