Selection for cold resistance alters gene transcript levels in Drosophila melanogaster

Telonis‐Scott, Marina; Hallas, Rebecca; McKechnie, Stephen William; Wee, Choon Wei; Hoffmann, Ary A.

doi:10.1016/j.jinsphys.2009.01.010

Cited by 75 publications

(82 citation statements)

References 40 publications

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“…Qin et al, 2005) or populations selected for their ability to recover from a single cold exposure (e.g. Telonis-Scott et al, 2009). For example, 37 candidate genes were identified after 30min of recovery at 25°C from a cold exposure of 0°C for 2h (Qin et al, 2005), whereas 94 differentially regulated genes were identified from a comparison of lines of flies selected for chill coma recovery (Telonis-Scott et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster

Zhang

Marshall

Westwood

et al. 2011

Journal of Experimental Biology

106

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SUMMARYInsects in the field are exposed to multiple bouts of cold, and there is increasing evidence that the fitness consequences of repeated cold exposure differ from the impacts of a single cold exposure. We tested the hypothesis that different kinds of cold exposure (in this case, single short, prolonged and repeated cold exposure) would result in differential gene expression. We exposed 3day old adult female wild-type Drosophila melanogaster (Diptera: Drosophilidae) to -0.5°C for a single 2h exposure, a single 10h exposure, or five 2h exposures on consecutive days, and extracted RNA after 6h of recovery. Global gene expression was quantified using an oligonucleotide microarray and validated with real-time PCR using different biological replicates. We identified 76 genes upregulated in response to multiple cold exposure, 69 in response to prolonged cold exposure and 20 genes upregulated in response to a single short cold exposure, with a small amount of overlap between treatments. Three genesTurandot A, Hephaestus and CG11374 -were upregulated in response to all three cold exposure treatments. Key functional groups upregulated include genes associated with muscle structure and function, the immune response, stress response, carbohydrate metabolism and egg production. We conclude that cold exposure has wide-ranging effects on gene expression in D. melanogaster and that increased duration or frequency of cold exposure has impacts different to those of a single short cold exposure. This has important implications for extrapolating laboratory studies of insect overwintering that are based on only a single cold exposure. Supplementary material available online at

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Section: Discussionmentioning

confidence: 99%

Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster

Zhang

Marshall

Westwood

et al. 2011

Journal of Experimental Biology

106

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“…At low temperatures, insects enter chill-coma, a reversible state of paralysis (3). The time taken to recover from this paralysis (chill-coma recovery time, CCR) is one of the most common metrics of insect cold tolerance (4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22) and has been used to develop and test theory in biogeography (5-9), evolution (10), and climate change biology (11,12). Variation in CCR reflects variation in low temperature exposure in the wild; for example, CCR is faster in individuals collected from populations or species at higher altitudes or latitudes, suggesting selection for faster recovery in cooler environments (4,5).…”

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confidence: 99%

“…Variation in CCR reflects variation in low temperature exposure in the wild; for example, CCR is faster in individuals collected from populations or species at higher altitudes or latitudes, suggesting selection for faster recovery in cooler environments (4,5). In Drosophila melanogaster, CCR can be modified in laboratory experiments through thermal acclimation (13,14) and artificial selection (e.g., [15][16][17][18][19].…”

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confidence: 99%

“…Genomic and transcriptomic screens (18)(19)(20)(21)(22)(23) have not identified consistent candidate loci that might explain variation in CCR. Although it is generally assumed that recovery of movement requires a reversal of the processes that led to onset of chillcoma, variation in CCR is not always accompanied by variation in chill-coma onset temperature (14).…”

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Reestablishment of ion homeostasis during chill-coma recovery in the cricketGryllus pennsylvanicus

MacMillan

Williams

Staples

et al. 2012

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

155

158

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The time required to recover from cold-induced paralysis (chill-coma) is a common measure of insect cold tolerance used to test central questions in thermal biology and predict the effects of climate change on insect populations. The onset of chill-coma in the fall field cricket (Gryllus pennsylvanicus, Orthoptera: Gryllidae) is accompanied by a progressive drift of Na + and water from the hemolymph to the gut, but the physiological mechanisms underlying recovery from chill-coma are not understood for any insect. Using a combination of gravimetric methods and atomic absorption spectroscopy, we demonstrate that recovery from chill-coma involves a reestablishment of hemolymph ion content and volume driven by removal of Na + and water from the gut. Recovery is associated with a transient elevation of metabolic rate, the time span of which increases with increasing cold exposure duration and closely matches the duration of complete osmotic recovery. Thus, complete recovery from chill-coma is metabolically costly and encompasses a longer period than is required for the recovery of muscle potentials and movement. These findings provide evidence that physiological mechanisms of hemolymph ion content and volume regulation, such as ion-motive ATPase activity, are instrumental in chill-coma recovery and may underlie natural variation in insect cold tolerance.ionoregulation | metabolism | osmotic homeostasis | thermal limits | stress resistance

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“…Collinge et al, 2008;Dennis et al, 2015), selection (e.g. Telonis-Scott et al, 2009;Williams et al, 2014) or phenotypic plasticity (MacMillan et al, 2016). Thus, insect cold tolerance is an ecologically important trait for which the mechanistic link from genotype to phenotype is poorly understood.…”

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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Selection for cold resistance alters gene transcript levels in Drosophila melanogaster

Cited by 75 publications

References 40 publications

Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster

Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster

Reestablishment of ion homeostasis during chill-coma recovery in the cricketGryllus pennsylvanicus

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

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