Chilled, starved or frozen: insect mitochondrial adaptations to overcome the cold

Lebenzon, Jacqueline E.; Overgaard, Johannes; Jørgensen, Lisa Bjerregaard

doi:10.1016/j.cois.2023.101076

Cited by 7 publications

(2 citation statements)

References 49 publications

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“…Temperature adaptation is an important factor in insect response to environmental change [51]; insects can adjust their own physiological and biochemical mechanisms by changing their cellular activity and metabolism to respond to changes in the external environment [52]. Cold stress is diverse, and different insect species have evolved different metabolic and physiological adaptations [53]. Maintaining cellular homeostasis, preserving cell viability and enhancing cellular tolerance by adjusting their metabolic status are the most important means of maintaining vital signs in insects at low temperatures [54].…”

Section: Discussionmentioning

confidence: 99%

Comparative Transcriptome Analysis of Galeruca daurica Reveals Cold Tolerance Mechanisms

Zhang,

Sun,

Zhang

et al. 2023

Genes

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Galeruca daurica (Joannis) is a pest species with serious outbreaks in the Inner Mongolian grasslands in recent years, and its larvae and eggs are extremely cold-tolerant. To gain a deeper understanding of the molecular mechanism of its cold-tolerant stress response, we performed de novo transcriptome assembly of G. daurica via RNA-Seq and compared the differentially expressed genes (DEGs) of first- and second-instar larvae grown and developed indoors and outdoors, respectively. The results show that cold tolerance in G. daurica is associated with changes in gene expression mainly involved in the glycolysis/gluconeogenesis pathway, the fatty acid biosynthesis pathway and the production of heat shock proteins (HSPs). Compared with the control group (indoor), the genes associated with gluconeogenesis, fatty acid biosynthesis and HSP production were up-regulated in the larvae grown and developed outdoors. While the changes in these genes were related to the physiological metabolism and growth of insects, it was hypothesized that the proteins encoded by these genes play an important role in cold tolerance in insects. In addition, we also investigated the expression of genes related to the metabolic pathway of HSPs, and the results show that the HSP-related genes were significantly up-regulated in the larvae of G. daurica grown and developed outdoors compared with the indoor control group. Finally, we chose to induce significant expression differences in the Hsp70 gene (Hsp70A1, Hsp70-2 and Hsp70-3) via RNAi to further illustrate the role of heat stress proteins in cold tolerance on G. daurica larvae. The results show that separate and mixed injections of dsHSP70A1, dsHsp70-2 and dsHsp70-3 significantly reduced expression levels of the target genes in G. daurica larvae. The super-cooling point (SCP) and the body fluid freezing point (FP) of the test larvae were determined after RNAi using the thermocouple method, and it was found that silencing the Hsp70 genes significantly increased the SCP and FP of G. daurica larvae, which validated the role of heat shock proteins in the cold resistance of G. daurica larvae. Our findings provide an important theoretical basis for further excavating the key genes and proteins in response to extremely cold environments and analyzing the molecular mechanism of cold adaptation in insects in harsh environments.

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Section: Discussionmentioning

confidence: 99%

Comparative Transcriptome Analysis of Galeruca daurica Reveals Cold Tolerance Mechanisms

Zhang,

Sun,

Zhang

et al. 2023

Genes

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“…Our understanding of how mitochondria in temperate and polar insects adapt to the winter season is still limited ( Lubawy et al, 2022 ; Lebenzon et al, 2023 ). Overwintering insects are exposed to low ambient temperatures and often spend the winter in diapause—a state of developmental arrest, behavioral inactivity, and deep metabolic suppression ( Koštál, 2006 ; Teets et al, 2023 ).…”

Section: Introductionmentioning

confidence: 99%

Extracellular freezing induces a permeability transition in the inner membrane of muscle mitochondria of freeze-sensitive but not freeze-tolerant Chymomyza costata larvae

Štětina,

Koštál

2024

Front. Physiol.

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Background: Many insect species have evolved the ability to survive extracellular freezing. The search for the underlying principles of their natural freeze tolerance remains hampered by our poor understanding of the mechanistic nature of freezing damage itself.Objectives: Here, in search of potential primary cellular targets of freezing damage, we compared mitochondrial responses (changes in morphology and physical integrity, respiratory chain protein functionality, and mitochondrial inner membrane (IMM) permeability) in freeze-sensitive vs. freeze-tolerant phenotypes of the larvae of the drosophilid fly, Chymomyza costata.Methods: Larvae were exposed to freezing stress at −30°C for 1 h, which is invariably lethal for the freeze-sensitive phenotype but readily survived by the freeze-tolerant phenotype. Immediately after melting, the metabolic activity of muscle cells was assessed by the Alamar Blue assay, the morphology of muscle mitochondria was examined by transmission electron microscopy, and the functionality of the oxidative phosphorylation system was measured by Oxygraph-2K microrespirometry.Results: The muscle mitochondria of freeze-tolerant phenotype larvae remained morphologically and functionally intact after freezing stress. In contrast, most mitochondria of the freeze-sensitive phenotype were swollen, their matrix was diluted and enlarged in volume, and the structure of the IMM cristae was lost. Despite this morphological damage, the electron transfer chain proteins remained partially functional in lethally frozen larvae, still exhibiting strong responses to specific respiratory substrates and transferring electrons to oxygen. However, the coupling of electron transfer to ATP synthesis was severely impaired. Based on these results, we formulated a hypothesis linking the observed mitochondrial swelling to a sudden loss of barrier function of the IMM.

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Cross-talk between low temperature and other environmental factors

Boardman

2024

Current Opinion in Insect Science

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Chilled, starved or frozen: insect mitochondrial adaptations to overcome the cold

Cited by 7 publications

References 49 publications

Comparative Transcriptome Analysis of Galeruca daurica Reveals Cold Tolerance Mechanisms

Comparative Transcriptome Analysis of Galeruca daurica Reveals Cold Tolerance Mechanisms

Extracellular freezing induces a permeability transition in the inner membrane of muscle mitochondria of freeze-sensitive but not freeze-tolerant Chymomyza costata larvae

Cross-talk between low temperature and other environmental factors

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