Insect cross-tolerance to freezing and drought stress: role of metabolic rearrangement

Abstract

The accumulation of trehalose has been suggested as a mechanism underlying insect cross-tolerance to cold/freezing and drought. Here we show that exposing diapausing larvae of the drosophilid fly, Chymomyza costata to dry conditions significantly stimulates their freeze tolerance. It does not, however, improve their tolerance to desiccation, nor does it significantly affect trehalose concentrations. Next, we use metabolomics to compare the complex alterations to intermediary metabolism pathways in response to three environmental factors with different ecological meanings: environmental drought (an environmental stressor causing mortality), decreasing ambient temperatures (an acclimation stimulus for improvement of cold hardiness), and short days (an environmental signal inducing diapause). We show that all three factors trigger qualitatively similar metabolic rearrangement and a similar phenotypic outcome—improved larval freeze tolerance. The similarities in metabolic response include (but are not restricted to) the accumulation of typical compatible solutes and the accumulation of energy-rich molecules (phosphagens). Based on these results, we suggest that transition to metabolic suppression (a state in which chemical energy demand is relatively low but need for stabilization of macromolecules is high) represents a common axis of metabolic pathway reorganization towards accumulation of non-toxic cytoprotective compounds, which in turn stimulates larval freeze tolerance.

Cross‐protection interactions in insect pests: Implications for pest management in a changing climate

“…69 Other biochemical compounds involved in cross-protection include the production of sugar alcohols, trehalose and proline, which serve as sources of metabolic energy in response to heat and starvation and protect biomolecules from freeze damage following exposure to low temperatures. 28,29,70 Genes associated with xenobiotic detoxification play a significant role in mediating tolerance to chemical stressors. In insects, detoxification genes, such as cytochrome P450s monooxygenases (CYPs), glutathione-S-transferases (GSTs) and esterases (ESTs), breakdown xenobiotic compounds and become overexpressed following exposure to insecticides, herbicides and plant defense compounds.…”

“…Decreases in ROS corresponded with low levels of citrate synthase, which is indicative of mitochondrial activity, suggesting that hypoxia facilitates irradiation tolerance by hindering mitochondrial respiration resulting in low ROS levels 69 . Other biochemical compounds involved in cross‐protection include the production of sugar alcohols, trehalose and proline, which serve as sources of metabolic energy in response to heat and starvation and protect biomolecules from freeze damage following exposure to low temperatures 28,29,70 …”

“…1(B) ). 26 , 27 , 28 , 29 , 30 , 31 , 32 These changes encompass a wide range of defensive strategies such as increases in antioxidants, metabolites, up‐regulation of molecular chaperones and detoxification enzymes, all of which help maintain the integrity and function of cellular processes important for survival. 26 , 27 , 28 , 29 , 30 , 31 , 32 For example, in the malt fly, Chymomyza costata , enhanced freeze tolerance following exposure to drought stress was linked to the accumulation of proline, glutamine, and trehalose; three sugar metabolites with cryoprotective properties known to stabilize the function of macromolecules.…”

“… 26 , 27 , 28 , 29 , 30 , 31 , 32 These changes encompass a wide range of defensive strategies such as increases in antioxidants, metabolites, up‐regulation of molecular chaperones and detoxification enzymes, all of which help maintain the integrity and function of cellular processes important for survival. 26 , 27 , 28 , 29 , 30 , 31 , 32 For example, in the malt fly, Chymomyza costata , enhanced freeze tolerance following exposure to drought stress was linked to the accumulation of proline, glutamine, and trehalose; three sugar metabolites with cryoprotective properties known to stabilize the function of macromolecules. 29 In addition to biochemical responses, shared responses may also arise from changes in transcriptional regulation or through epigenetic modifications, molecular changes that regulate the expression of genes without altering the DNA sequence, potentially serving as another driving force behind cross‐protection (Fig.…”

“… 26 , 27 , 28 , 29 , 30 , 31 , 32 For example, in the malt fly, Chymomyza costata , enhanced freeze tolerance following exposure to drought stress was linked to the accumulation of proline, glutamine, and trehalose; three sugar metabolites with cryoprotective properties known to stabilize the function of macromolecules. 29 In addition to biochemical responses, shared responses may also arise from changes in transcriptional regulation or through epigenetic modifications, molecular changes that regulate the expression of genes without altering the DNA sequence, potentially serving as another driving force behind cross‐protection (Fig. 1(D) ).…”