Determination of water “bound” by soluble subcellular components during low-temperature acclimation in the gall fly larva, Eurosta solidagensis

Storey, Kenneth B.; Baust, John G.; Buescher, Philip

doi:10.1016/0011-2240(81)90104-8

Cited by 72 publications

(42 citation statements)

References 17 publications

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“…Proline can be up-or down-regulated to prevent changes in cellular water content in response to changing osmotic concentration in the cell environment (29,30). Thus, high proline levels may reduce the freeze concentration of intracellular fluids during extracellular freezing (11,31). We found that feeding the fruit fly larvae proline-augmented diet had no statistically significant effects on the larval whole-body osmotic balance.…”

Section: Feeding Larvae Proline-augmented Diet Results In Accumulatiomentioning

confidence: 80%

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.

138

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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: Feeding Larvae Proline-augmented Diet Results In Accumulatiomentioning

confidence: 80%

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.

138

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“…Water content influences the supercooling capacity of freezingsusceptible species, and in freezing tolerant ones a proportion of body water remains unfrozen in order to allow a low level basal metabolism (Block, 2003). Thus, one of the key features that has been rarely studied in arthropods is the capacity to bind water molecules (Storey et al, 1981;Storey, 1983). In our study, we used an original non-invasive protocol to determine the relative bound water content in crustacean bodies by proton NMR transverse relaxation measurements performed on the whole live organisms.…”

Section: Discussionmentioning

confidence: 99%

“…The bound water is the water that is so closely associated with cellular or other components in an organism that it is not available to participate in the freezing processes (Hazelwood, 1977). The bound water content of the freeze-tolerant larvae of Eurosta solidaginis increased with cold acclimation (Storey et al, 1981), and this was due to changes in water binding by cryoprotectants and macromolecules (mainly glycogen and proteins). In freezetolerant species, bound water will not participate in ice formation and this results in non-freezable shells of water surrounding cellular components, protecting them from the denaturation due to freezing dehydration (Storey et al, 1981).…”

Section: Introductionmentioning

confidence: 99%

Freezing or supercooling: how does an aquatic subterranean crustacean survive exposures at subzero temperatures?

Issartel

Voituron

Odagescu

et al. 2006

Journal of Experimental Biology

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Crystallization temperature (T c ), resistance to inoculative freezing (IF), ice contents, bound water, protein and glycogen body contents were measured in the aquatic subterranean crustacean Niphargus rhenorhodanensis and in the morphologically close surface-dwelling aquatic crustacean Gammarus fossarum, both acclimated at 12°C, 3°C and -2°C. Cold acclimation induced an increase in the T c values in both species but no survival was observed after thawing. However, after inoculation at high sub-zero temperatures, cold-acclimated N. rhenorhodanensis survived whereas all others, including the 3°C and -2°C acclimated G. fossarum died. In its aquatic environment, N. rhenorhodanensis is likely to encounter inoculative freezing before reaching the T c and IF tolerance appears as a highly adaptive trait in this species. Bound water and glycogen were found to increase in the 3°C and -2°C acclimated N. rhenorhodanensis, whereas no variation was observed in G. fossarum. Considering the hydrophilic properties of glycogen, such a rise may be correlated with the increased bound water measured in cold-acclimated N. rhenorhodanensis, and may be linked to the survival of this species when it was inoculated. The ecological significance of the survival of the aquatic subterranean crustacean to inoculative freezing is paradoxical, as temperature is currently highly buffered in its habitat. However, we assume that past geographical distribution and resulting life history traits of N. rhenorhodanensis are key parameters in the current cold-hardiness of the species.

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“…In winter, E. solidaginis larvae employ a multicomponent cryoprotectant system, primarily composed of glycerol, sorbitol and trehalose, that collectively can produce a hemolymph osmolality of 900mOsm or higher (Baust and Lee, 1981;Storey et al, 1981;Williams et al, 2004). We chose to measure glycerol levels because it is the predominant cryoprotectant accumulated at this time of the year, and its synthesis is associated with plant senescence and the drying of gall tissues in autumn (Rojas et al, 1986).…”

Section: Discussionmentioning

confidence: 99%

Mild desiccation rapidly increases freeze tolerance of the goldenrod gall fly, Eurosta solidaginis: evidence for drought-induced RCH

Levis

Lee

2012

Journal of Experimental Biology

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SUMMARYOverwintering insects may experience extreme cold and desiccation stress. Both freezing and desiccation require cells to tolerate osmotic challenge as solutes become concentrated in the hemolymph. Not surprisingly, physiological responses to low temperature and desiccation share common features and may confer cross-tolerance against these stresses. Freeze-tolerant larvae of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae), experience extremely dry and cold conditions in winter. To determine whether mild desiccation can improve freeze tolerance at organismal and cellular levels, we assessed survival, hemolymph osmolality and glycerol levels of control and desiccated larvae. Larvae that lost only 6-10% of their body mass, in as little as 6h, had markedly higher levels of freeze tolerance. Mild, rapid desiccation increased freezing tolerance at -15°C in September-collected larvae (33.3±6.7 to 73.3±12%) and at -20°C in October-collected larvae (16.7±6.7 to 46.7±3.3%). Similarly, 6h of desiccation improved in vivo survival by 17-43% in fat body, Malpighian tubule, salivary gland and tracheal cells at -20°C. Desiccation also enhanced intrinsic levels of cold tolerance in midgut cells frozen ex vivo (38.7±4.6 to 89.2±5.5%). Whereas hemolymph osmolality increased significantly with desiccation treatment from 544±16 to 720±26mOsm, glycerol levels did not differ between control and desiccated groups. The rapidity with which a mild desiccation stress increased freeze tolerance closely resembles the rapid cold-hardening response, which occurs during brief sub-lethal chilling, and suggests that drought stress can induce rapid cold-hardening.

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Determination of water “bound” by soluble subcellular components during low-temperature acclimation in the gall fly larva, Eurosta solidagensis

Cited by 72 publications

References 17 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

Freezing or supercooling: how does an aquatic subterranean crustacean survive exposures at subzero temperatures?

Mild desiccation rapidly increases freeze tolerance of the goldenrod gall fly, Eurosta solidaginis: evidence for drought-induced RCH

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