Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: Role of ion homeostasis

Košťál, Vladimı́r; Renault, David; Mehrabianova, Aneta; Bastl, J.

doi:10.1016/j.cbpa.2006.12.033

Cited by 138 publications

(113 citation statements)

References 33 publications

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“…In addition, we transferred fully grown 15°C-acclimated larvae to a FTR where temperature oscillated daily: 6°C∕11°C (12 h∕12 h) under constant darkness for 3 d (treatment iii.). Under an FTR, most larvae were in a dormant state (quiescence) with their development halted and chill injury and mortality of larvae was prevented (23)(24)(25). We examined the capacity for freeze tolerance in D. melanogaster larvae under various treatments, by assessing their ability to survive after being gradually frozen to −5°C in the presence of surrounding ice and then gradually melted (see Materials and Methods for details).…”

Section: Resultsmentioning

confidence: 99%

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Košťál

Šimek

Zahradníčková

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

140

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Among vertebrates, only a few species of amphibians and reptiles tolerate the formation of ice crystals in their body fluids. Freeze tolerance is much more widespread in invertebrates, especially in overwintering insects. Evolutionary adaptations for freeze tolerance are considered to be highly complex. Here we show that surprisingly simple laboratory manipulations can change the chill susceptible insect to the freeze tolerant one. Larvae of Drosophila melanogaster, a fruit fly of tropical origin with a weak innate capacity to tolerate mild chilling, can survive when approximately 50% of their body water freezes. To achieve this goal, synergy of two fundamental prerequisites is required: (i) shutdown of larval development by exposing larvae to low temperatures (dormancy) and (ii) incorporating the free amino acid proline in tissues by feeding larvae a proline-augmented diet (cryopreservation).insect cold tolerance | long-term storage | metabolomics | cryoprotection | quiescence T he vast majority of insect lineages and species evolved, diversified, and recently live in warm lowland tropics, where seasonal and daily temperatures fluctuate little. This scenario is also true for the genus Drosophila, which contains almost 1,500 described species (1) including a common model of modern biology, the fruit fly Drosophila (Sophophora) melanogaster (Meigen, 1830) (fruit fly in further text). The ancestral members of this genus were adapted to warm temperatures (2), and most of the extant species still have tropical and/or subtropical distributions and are chill susceptible (3). The immature development of D. melanogaster halts at temperatures below 10°C (4), chill injury occurs below 6°C (5), and all developmental stages die when chilled (supercooled) below −5°C for just a few hours (6). The ability to tolerate freezing; i.e., formation of ice crystals in body fluids, is unknown in any Drosophila species (2, 5).Numerous insect lineages, including some drosophilid flies, colonized colder environments in higher altitudes or temperate and polar regions. Such lineages had to overcome selection pressures of shorter growing season, exaggerated daily temperature fluctuations, and seasonal drop of temperatures below the physiological thresholds for activity, growth, and development (7). It is now widely accepted that cold adaptation in insects is highly complex and requires adjustments at all levels of biological organization (8-16). Supercooling and freeze tolerance are two main strategies that help insects to cope with the risk of water freezing in a cryothermic state. While the capacity for supercooling seems to be basal in cold-adapted arthropod lineages, freeze tolerance probably converged in several groups in response to either severe Arctic winters or unpredictable subzero temperature events typical of cold habitats in the southern hemisphere (17, 18). For example, larvae of subarctic drosophilid fly, Chymomyza costata (Zetterstedt, 1838) are extremely freeze tolerant and may even survive after submergence in liquid nitro...

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Section: Resultsmentioning

confidence: 99%

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Košťál

Šimek

Zahradníčková

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

140

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“…Such patterns imply that interactions between the hemolymph and tissues other than muscle may be driving the loss of muscle equilibrium potentials during cooling. Studies that have addressed the loss of ion balance during cooling have exclusively measured ion concentrations or their effects on muscle potential, and thus have overlooked the potential for interactive effects of tissue or hemolymph water content and ion abundance (Goller and Esch, 1990;Hosler et al, 2000;Kostál et al, 2004;Kostál et al, 2006;Kostál et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the fall field cricket,Gryllus pennsylvanicus

MacMillan

Sinclair

2011

Journal of Experimental Biology

153

176

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SUMMARYTo predict the effects of changing climates on insect distribution and abundance, a clear understanding of the mechanisms that underlie critical thermal limits is required. In insects, the loss of muscle function and onset of cold-induced injury has previously been correlated with a loss of muscle resting potential. To determine the cause of this loss of function, we measured the effects of cold exposure on ion and water homeostasis in muscle tissue, hemolymph and the alimentary canal of the fall field cricket, Gryllus pennsylvanicus, during an exposure to 0°C that caused chilling injury and death. Low temperature exposure had little effect on muscle osmotic balance but it dissipated muscle ion equilibrium potentials through interactions between the hemolymph and gut. Hemolymph volume declined by 84% during cold exposure whereas gut water content rose in a comparable manner. This rise in water content was driven by a failure to maintain osmotic equilibrium across the gut wall, which resulted in considerable migration of Na + , Ca 2+ and Mg 2+ into the alimentary canal during cold exposure. This loss of homeostasis is likely to be a primary mechanism driving the cold-induced loss of muscle excitability and progression of chilling injury in chill-susceptible insect species.Supplementary material available online at

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“…Extreme chilling (see Box 1 for terminology) may cause tissue damage either directly, for example, as a result of brief (minutes or hours) exposures to extreme cold (but not freezing) temperatures, or indirectly, over more extended periods at less extreme cold, by interrupting key physiological processes at tissue and organ level (Costanzo and Lee, 2013; Denlinger and Lee, 2010;Knight and Knight, 2012). Chilling injury of insects has been repeatedly linked with a breakdown of diffusion barriers, collapse of ion gradients and loss of ion homeostasis; potassium concentration increases within the haemolymph, with decreases in both sodium and magnesium ions (Kostál et al, 2007;Kostál et al, 2006;Kostál et al, 2004). The progressive disruption to electrochemical gradients of ions eventually causes debilitation at the organ and whole-animal level, leading to loss of neuromuscular coordination and cessation of respiratory movements, as also occurs in fish (Friedlander et al, 1976).…”

Section: Introductionmentioning

confidence: 99%

“…They suggest that the damage that builds up during chill exposure can be either prevented or repaired by molecular processes that are either activated before the imposition of chill stress or re-activated during warming periods. For example, ion gradients are re-established (Kostál et al, 2007), heat shock proteins (HSPs) or other cytoskeletal components (Michaud and Denlinger, 2004) are upregulated, depleted energy reserves (Cheng-Ping and Denlinger, 1992) are recharged, and accumulated toxic metabolites are removed (Colinet et al, 2007). Induced resistance to freeze stress has a substantial research literature mainly focused on the induced production of compatible solutes displaying colligative properties or of 'antifreeze' or ice nucleation proteins (Costanzo and Lee, 2013).…”

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confidence: 99%

Molecular basis of chill resistance adaptations in poikilothermic animals

Hayward

Manso

Cossins

2014

Journal of Experimental Biology

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Chill and freeze represent very different components of low temperature stress. Whilst the principal mechanisms of tissue damage and of acquired protection from freeze-induced effects are reasonably well established, those for chill damage and protection are not. Non-freeze cold exposure (i.e. chill) can lead to serious disruption to normal life processes, including disruption to energy metabolism, loss of membrane perm-selectivity and collapse of ion gradients, as well as loss of neuromuscular coordination. If the primary lesions are not relieved then the progressive functional debilitation can lead to death. Thus, identifying the underpinning molecular lesions can point to the means of building resistance to subsequent chill exposures. Researchers have focused on four specific lesions: (i) failure of neuromuscular coordination, (ii) perturbation of bio-membrane structure and adaptations due to altered lipid composition, (iii) protein unfolding, which might be mitigated by the induced expression of compatible osmolytes acting as 'chemical chaperones ', (iv) or the induced expression of protein chaperones along with the suppression of general protein synthesis. Progress in all these potential mechanisms has been ongoing but not substantial, due in part to an over-reliance on straightforward correlative approaches. Also, few studies have intervened by adoption of single gene ablation, which provides much more direct and compelling evidence for the role of specific genes, and thus processes, in adaptive phenotypes. Another difficulty is the existence of multiple mechanisms, which often act together, thus resulting in compensatory responses to gene manipulations, which may potentially mask disruptive effects on the chill tolerance phenotype. Consequently, there is little direct evidence of the underpinning regulatory mechanisms leading to induced resistance to chill injury. Here, we review recent advances mainly in lower vertebrates and in arthropods, but increasingly in genetic model species from a broader range of taxa. KEY WORDS: Membrane fluidity, Proteostasis, Compatible solutes, Gene ablation IntroductionEnvironmental cold poses multiple problems for all living organisms, especially poikilotherms (Cossins and Bowler, 1987). The effects of low temperature on performance are largely determined by the extent to which cooling reduces the rate of biochemical reactions -thus slowing down any rate-dependent processes (Hochachka and Somero, 2002). The impact on survival, however, is determined by the disruptive effects of extreme cold on *Author for correspondence (cossins@liverpool.ac.uk) the molecular processes underpinning normal cellular function, such as protein and membrane integrity, which in turn are closely associated with such fundamental cellular properties such as ion homeostasis and continued activity of excitable cells (Lee, 2010). Thus, at some point during both declining temperatures and diminishing performance, cold becomes stressful, and chilling injuries then accumulate over time, leading...

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Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: Role of ion homeostasis

Cited by 138 publications

References 33 publications

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the fall field cricket,Gryllus pennsylvanicus

Molecular basis of chill resistance adaptations in poikilothermic animals

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