The Integrative Physiology of Insect Chill Tolerance

Overgaard, Johannes; MacMillan, Heath A.

doi:10.1146/annurev-physiol-022516-034142

Cited by 308 publications

(426 citation statements)

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“…Chill-susceptible insects are those that succumb to the effects of chilling at temperatures 46 well above the freezing point of their body fluids (Bale, 1996;Overgaard and MacMillan, 2017). 47…”

Section: Chill Susceptibility In Insects 45mentioning

confidence: 99%

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Yerushalmi

Misyura

MacMillan

et al. 2017

Preprint

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(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/224832 doi: bioRxiv preprint first posted online 2 Abstract 22At low temperatures, Drosophila, like most insects, lose the ability to regulate ion and water 23 balance across the gut epithelia, which can lead to a lethal increase of [K + ] in the hemolymph 24 (hyperkalemia). Cold-acclimation, the physiological response to low temperature exposure, can 25 mitigate or entirely prevent these ion imbalances, but the physiological mechanisms that 26 facilitate this process are not well understood. Here, we test whether plasticity in the 27 ionoregulatory physiology of the gut and Malpighian tubules of Drosophila may aid in 28 preserving ion homeostasis in the cold. Upon adult emergence, D. melanogaster females were 29 subjected to seven days at warm (25°C) or cold (10°C) acclimation conditions. The cold 30 acclimated flies had a lower critical thermal minimum (CTmin), recovered from chill coma more 31 quickly, and better maintained hemolymph K + balance in the cold. The improvements in chill 32 tolerance coincided with increased Malpighian tubule fluid secretion and better maintenance of 33 K + secretion rates in the cold, as well as reduced rectal K + reabsorption in cold-acclimated flies. 34To test whether modulation of ion-motive ATPases, the main drivers of epithelial transport in the 35 alimentary canal, mediate these changes, we measured the activities of Na + -K + -ATPase and V-36 type H + -ATPase at the Malpighian tubules, midgut, and hindgut. Na + /K + -ATPase and V-type H + -37ATPase activities were lower in the midgut and the Malpighian tubules of cold-acclimated flies, 38 but unchanged in the hindgut of cold acclimated flies, and were not predictive of the observed 39 alterations in K + transport. Our results suggest that modification of Malpighian tubule and gut 40 ion and water transport likely prevents cold-induced hyperkalemia in cold-acclimated flies and 41 that this process is not directly related to the activities of the main drivers of ion transport in 42 these organs, Na + /K + -and V-type H + -ATPases. 43All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Section: Chill Susceptibility In Insects 45mentioning

confidence: 99%

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Yerushalmi

Misyura

MacMillan

et al. 2017

Preprint

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“…During this cold-induced coma, chill-sensitive insects will accumulate cold injury in a manner that is generally dependent on the intensity and duration of the cold stress (Nedveď et al, 1998;Koštál et al, 2004;MacMillan and Sinclair, 2011a;Overgaard and MacMillan, 2017). Sensitivity to such cold stress varies enormously amongst insect species adapted to different thermal environments, and accordingly insect cold tolerance is often found to correlate closely with species distribution (Addo-Bediako et al, 2000;Bale, 2002;Kimura, 2004;Sunday et al, 2011;Kellermann et al, 2012;Andersen et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

“…Several acclimation studies have now observed that cold-acclimated insects either partially or completely retain K + balance during cold stress, and thereby avoid injury (Koštál et al, 2004(Koštál et al, , 2006Coello Alvarado et al, 2015;MacMillan et al, 2015a,b). A corollary of these observations is that cold-acclimated insects better preserve V m through improved maintenance of K + balance (Koštál et al, 2004;Overgaard and MacMillan, 2017), which in turn prevents cell death and thus ensures organismal survival. This hypothesis, however, remains to be examined directly.…”

Section: Introductionmentioning

confidence: 99%

Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Andersen

Folkersen

MacMillan

et al. 2016

Journal of Experimental Biology

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Most insects have the ability to alter their cold tolerance in response to temporal temperature fluctuations, and recent studies have shown that insect cold tolerance is closely tied to the ability to maintain transmembrane ion gradients that are important for the maintenance of cell membrane potential (V m ). Several studies have therefore suggested a link between preservation of V m and cellular survival after cold stress, but none has measured V m in this context. We tested this hypothesis by acclimating locusts (Locusta migratoria) to high (31°C) and low temperature (11°C) for 4 days before exposing them to cold stress (0°C) for up to 48 h and subsequently measuring ion balance, cell survival, muscle V m , and whole animal performance. Cold stress caused gradual muscle cell death, which coincided with a loss of ion balance and depolarization of muscle V m . The loss of ion balance and cell polarization were, however, dampened markedly in cold-acclimated locusts such that the development of chill injury was reduced. To further examine the association between cellular injury and V m we exposed in vitro muscle preparations to cold buffers with low, intermediate, or. These experiments revealed that cellular injury during cold exposure occurs when V m becomes severely depolarized. Interestingly, we found that cellular sensitivity to hypothermic hyperkalaemia was lower in cold-acclimated locusts that were better able to defend V m whilst exposed to high extracellular [K + ]. Together these results demonstrate a mechanism of cold acclimation in locusts that improves survival after cold stress: increased cold tolerance is accomplished by preservation of V m through maintenance of ion homeostasis and decreased K + sensitivity.

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“…Because Fst is encoded in an intron of Dh-44, a gene that may have a role in water balance and therefore cold tolerance (Terhzaz et al, 2015;Overgaard and Macmillan, 2017), we measured Dh-44 expression patterns in our mutant lines. Fst and Dh-44 expression are not correlated, and we show that the expression of Dh-44 is unaffected by Fst deletion or by insertion of w + in the Fst locus.…”

Section: Frost Is Not Necessary For Cold Tolerancementioning

confidence: 99%

“…Ectotherm cold tolerance strategies are well described (Lee, 2010;Sinclair et al, 2015), and a number of low molecular weight cryoprotectants are associated with surviving sub-zero temperatures, such as glycerol, trehalose and proline, and ice-binding proteins, such as antifreeze proteins (Zachariassen and Kristiansen, 2000;Bale and Hayward, 2010;Storey and Storey, 2013). In addition, the role of maintaining ion and water balance (and recovering homeostasis post-cold exposure) in cold hardiness is reasonably well understood (Overgaard and Macmillan, 2017). Although genes covering a broad range of functions appear to be associated with increased cold tolerance, surprisingly, few of these genes have been shown to have a function in cold tolerance.…”

Section: Introductionmentioning

confidence: 99%

CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

Newman

Toxopeus

Udaka

et al. 2017

Journal of Experimental Biology

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The ability to survive and reproduce after cold exposure is important in all kingdoms of life. However, even in a sophisticated genetic model system like Drosophila melanogaster, few genes have been identified as functioning in cold tolerance. The accumulation of the Frost (Fst) gene transcript increases after cold exposure, making it a good candidate for a gene that has a role in cold tolerance. Despite extensive RNAi knockdown analysis, no role in cold tolerance has been assigned to Fst. CRISPR is an effective technique for completely knocking down genes, and is less likely to produce offtarget effects than GAL4-UAS RNAi systems. We have used CRISPR-mediated homologous recombination to generate Fst-null alleles, and these Fst alleles uncovered a requirement for FST protein in maintaining female fecundity following cold exposure. However, FST does not have a direct role in survival following cold exposure. FST mRNA accumulates in the Malpighian tubules, and the FST protein is a highly disordered protein with a putative signal peptide for export from the cell. Future work is needed to determine whether FST is exported from the Malpighian tubules and directly interacts with female reproductive tissues post-cold exposure, or whether it is required for other repair/recovery functions that indirectly alter energy allocation to reproduction.

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The Integrative Physiology of Insect Chill Tolerance

Cited by 308 publications

References 144 publications

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

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