Adaptations to overwintering in the earthworm Dendrobaena octaedra: Genetic differences in glucose mobilisation and freeze tolerance

Holmstrup, Martin; Overgaard, Johannes; Bindesbøl, Anne-Mette; Pertoldi, Cino; Bayley, Mark

doi:10.1016/j.soilbio.2007.05.018

Cited by 31 publications

(7 citation statements)

References 31 publications

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“…Furthermore, the high levels of glucose, maltose, inositol, mannitol, sorbitol, and gluconolactone indicated that the pentose phosphate pathway was boosted in D females. As far as we know, earthworms and amphibians are the only animal groups that utilize glucose as their primary cryoprotectant [52], [53], although this osmolyte may have some potential disadvantages [54]. In the fruit fly Drosophila melanogaster , even though glucose was hypothesized to have a role in the rapid cold hardening response [55], the quantity of glucose was not related to the level of basal thermo-tolerance of flies [56].…”

Section: Discussionmentioning

confidence: 99%

Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

et al. 2013

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Diapause is a common feature in several arthropod species that are subject to unfavorable growing seasons. The range of environmental cues that trigger the onset and termination of diapause, in addition to associated hormonal, biochemical, and molecular changes, have been studied extensively in recent years; however, such information is only available for a few insect species. Diapause and cold hardening usually occur together in overwintering arthropods, and can be characterized by recording changes to the wealth of molecules present in the tissue, hemolymph, or whole body of organisms. Recent technological advances, such as high throughput screening and quantification of metabolites via chromatographic analyses, are able to identify such molecules. In the present work, we examined the survival ability of diapausing and non-diapausing females of the two-spotted spider mite, Tetranychus urticae, in the presence (0 or 5°C) or absence of cold acclimation. Furthermore, we examined the metabolic fingerprints of these specimens via gas chromatography-mass spectrophotometry (GC-MS). Partial Least Square Discriminant Analysis (PLS-DA) of metabolites revealed that major metabolic variations were related to diapause, indicating in a clear cut-off between diapausing and non-diapausing females, regardless of acclimation state. Signs of metabolic depression were evident in diapausing females, with most amino acids and TCA cycle intermediates being significantly reduced. Out of the 40 accurately quantified metabolites, seven metabolites remained elevated or were accumulated in diapausing mites, i.e. cadaverine, gluconolactone, glucose, inositol, maltose, mannitol and sorbitol. The capacity to accumulate winter polyols during cold-acclimation was restricted to diapausing females. We conclude that the induction of increased cold hardiness in this species is associated with the diapause syndrome, rather than being a direct effect of low temperature. Our results provide novel information about biochemical events related to the cold hardening process in the two-spotted spider mite.

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Section: Discussionmentioning

confidence: 99%

Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

et al. 2013

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“…Among temperate ectotherms, the degree of freeze tolerance in terms of minimum tolerable temperature and maximal duration can vary substantially among geographically distinct populations of conspecifics (Williams & Lee, ). Cryoprotectant accumulation is an important factor underpinning this variability, with northern populations typically achieving higher cryoprotectant levels during freezing than more southerly counterparts (Irwin & Lee, ; Holmstrup et al ., ; Costanzo et al ., ). In R. sylvatica , the glycemic response is critical in freeze tolerance, and whereas freezing‐induced glycogenolysis is well described (Storey & Storey, ), little is known about the role of transport proteins in glucose distribution to nonhepatic tissues.…”

Section: Discussionmentioning

confidence: 99%

Seasonal variation and freezing response of glucose transporter 2 in liver of the wood frog: implications for geographic variation in freeze tolerance

2015

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Subarctic populations of the wood frog Rana sylvatica survive freezing to temperatures at least 10-13°C below those of more southerly conspecifics. This profound freeze tolerance is due in part to an enhanced glucosic cryoprotectant system that requires rapid mobilization of glucose from hepatocytes during the early hours of freezing. To determine if glucose transporter 2 (GLUT2) in the liver contributes to geographic variation in freeze tolerance, we examined changes in the protein's abundance seasonally and in response to experimental freezing in frogs from Interior Alaska and southern Ohio, USA. Using immunoblotting techniques, we found that GLUT2 abundance increased in preparation for winter in both populations, but tests with Ohioan frogs showed that that altered temperature alone does not cause these seasonal changes. In Ohioan frogs, transporter expression apparently was regulated transcriptionally, as mRNA levels, assessed using quantitative real-time polymerase chain reaction, changed in accordance with protein abundance. However, this pattern was not observed in Alaskan frogs, suggesting that other mechanisms of regulation are important in this phenotype. Overall, GLUT2 abundance was constitutively greater and more responsive to freezing in Alaskan R. sylvatica, suggesting that GLUT2 contributes substantively to the extreme freeze tolerance of subarctic wood frogs.

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“…Furthermore, the high levels of glucose, maltose, inositol, mannitol, sorbitol, and gluconolactone indicated that the pentose phosphate pathway was boosted in D females. As far as we know, earthworms and amphibians are the only animal groups that utilize glucose as their primary cryoprotectant [52,53], although this osmolyte may have some potential disadvantages [54]. In the fruit fly Drosophila melanogaster, even though glucose was hypothesized to have a role in the rapid cold hardening response [55], the quantity of glucose was not related to the level of basal thermotolerance of flies [56].…”

Section: The Galactose Pathway Was Boosted For the Production Of Polyols In Diapausing Femalesmentioning

confidence: 99%

Correction: Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

Khodayari¹,

Moharramipour²,

Larvor³

et al. 2013

PLoS ONE

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Diapause is a common feature in several arthropod species that are subject to unfavorable growing seasons. The range of environmental cues that trigger the onset and termination of diapause, in addition to associated hormonal, biochemical, and molecular changes, have been studied extensively in recent years; however, such information is only available for a few insect species. Diapause and cold hardening usually occur together in overwintering arthropods, and can be characterized by recording changes to the wealth of molecules present in the tissue, hemolymph, or whole body of organisms. Recent technological advances, such as high throughput screening and quantification of metabolites via chromatographic analyses, are able to identify such molecules. In the present work, we examined the survival ability of diapausing and nondiapausing females of the two-spotted spider mite, Tetranychus urticae, in the presence (0 or 5uC) or absence of cold acclimation. Furthermore, we examined the metabolic fingerprints of these specimens via gas chromatography-mass spectrophotometry (GC-MS). Partial Least Square Discriminant Analysis (PLS-DA) of metabolites revealed that major metabolic variations were related to diapause, indicating in a clear cut-off between diapausing and non-diapausing females, regardless of acclimation state. Signs of metabolic depression were evident in diapausing females, with most amino acids and TCA cycle intermediates being significantly reduced. Out of the 40 accurately quantified metabolites, seven metabolites remained elevated or were accumulated in diapausing mites, i.e. cadaverine, gluconolactone, glucose, inositol, maltose, mannitol and sorbitol. The capacity to accumulate winter polyols during cold-acclimation was restricted to diapausing females. We conclude that the induction of increased cold hardiness in this species is associated with the diapause syndrome, rather than being a direct effect of low temperature. Our results provide novel information about biochemical events related to the cold hardening process in the two-spotted spider mite.

show abstract

Adaptations to overwintering in the earthworm Dendrobaena octaedra: Genetic differences in glucose mobilisation and freeze tolerance

Cited by 31 publications

References 31 publications

Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

Seasonal variation and freezing response of glucose transporter 2 in liver of the wood frog: implications for geographic variation in freeze tolerance

Correction: Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae

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