Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome

Abstract

Cold tolerance is a key determinant of insect distribution and abundance, and thermal acclimation can strongly influence organismal stress tolerance phenotypes, particularly in small ectotherms like Drosophila. However, there is limited understanding of the molecular and biochemical mechanisms that confer such impressive plasticity. Here, we use high-throughput mRNA sequencing (RNA-seq) and liquid chromatography – mass spectrometry (LC-MS) to compare the transcriptomes and metabolomes of D. melanogaster acclimated as adults to warm (rearing) (21.5 °C) or cold conditions (6 °C). Cold acclimation improved cold tolerance and led to extensive biological reorganization: almost one third of the transcriptome and nearly half of the metabolome were differentially regulated. There was overlap in the metabolic pathways identified via transcriptomics and metabolomics, with proline and glutathione metabolism being the most strongly-supported metabolic pathways associated with increased cold tolerance. We discuss several new targets in the study of insect cold tolerance (e.g. dopamine signaling and Na+-driven transport), but many previously identified candidate genes and pathways (e.g. heat shock proteins, Ca2+ signaling, and ROS detoxification) were also identified in the present study, and our results are thus consistent with and extend the current understanding of the mechanisms of insect chilling tolerance.

Antagonistic pleiotropy and mutation accumulation contribute to age‐related decline in stress response

“…For example, Cht2 was previously associated with cold acclimation response (MacMillan et al. ) and was associated with four‐week starvation resistance in this study. Meltrin , associated with one‐week starvation resistance in our study, was previously associated with cold acclimation response and age‐specific fitness (Durham et al.…”

“…; MacMillan et al. ). CG10916 , associated with four‐week nonacclimation survival in our study, was previously associated with determination of adult lifespan as well as cold acclimation (Paik et al.…”

Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

“…Likewise, the detection of precipitation‐associated outliers in genes relating to Malpighian tubule development, digestive tract, and tissue/ion homeostasis is consistent with other studies of desiccation in insects (Lemaitre & Miguel‐Aliaga, ; Liu et al, ; Telonis‐Scott et al, ) and suggests that genes relating to water‐solute balance could be important targets of selection from selection across a species ranges. Altogether, results suggest that investigating intraspecific variation in the physiology of water loss or storage in bumble bees could be a valuable avenue for future research, especially given that many of these precipitation associated processes have potentially overlapping functions with thermal tolerance (MacMillan et al, ).…”

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

“…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.…”

“…This RCH also preserves reproductive behavior (Shreve et al, 2004). The molecular underpinnings of Drosophila cold tolerance have been explored extensively via microarrays (Qin et al, 2005;Zhang et al, 2011), quantitative trait loci (QTL) (Morgan and Mackay, 2006;Gerken et al, 2015), RNA sequencing (MacMillan et al, 2016) and proteomics (Sørensen et al, 2017), yet surprisingly few genes are consistently upregulated or associated with low temperatures.…”