Physiological mechanisms of seasonal and rapid cold‐hardening in insects
TL;DR: A synthesis of the current literature suggests that these two forms of cold‐hardening may be more mechanistically distinct than originally anticipated.
Abstract: Insects have evolved a number of physiological mechanisms for coping with the detrimental effects of low temperature. As autumn progresses, insects use environmental signals such as shortening day lengths and gradually decreasing temperatures to trigger seasonal cold-hardening adaptations. These mechanisms include dramatic changes in biochemistry, cell function and gene expression that permit improved cell function and viability at low temperature. Insects are also capable of enhancing cold tolerance on a much shorter time scale, in a process called rapid cold-hardening (RCH). Rapid cold-hardening allows insects to improve cold tolerance almost instantaneously (i.e. within minutes to hours) to cope with sudden cold snaps and regularly-occurring diurnal drops in temperature. Initially, it was assumed that RCH would share many of the same basic mechanisms as seasonal cold-hardening, albeit on a shorter time scale. Although there is some evidence supporting this, recent work has called into question some of the original hypotheses concerning the mechanisms of RCH. Also, some mechanisms important for seasonal cold-hardening, such as up-regulation of stress proteins, are unlikely to function at the temperatures and time scales at which RCH occurs. In the present review, the current understanding of the physiological mechanisms governing both seasonal cold-hardening and RCH are summarized. A synthesis of the current literature suggests that these two forms of cold-hardening may be more mechanistically distinct than originally anticipated.
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TL;DR: Fuctuating temperatures could be used to enhance or weaken insects in applied rearing programs, and any prediction of insect performance in the field-including models of climate change or population performance-must account for the effect of fluctuating temperatures.
Abstract: All climate change scenarios predict an increase in both global temperature means and the magnitude of seasonal and diel temperature variation. The nonlinear relationship between temperature and biological processes means that fluctuating temperatures lead to physiological, life history, and ecological consequences for ectothermic insects that diverge from those predicted from constant temperatures. Fluctuating temperatures that remain within permissive temperature ranges generally improve performance. By contrast, those which extend to stressful temperatures may have either positive impacts, allowing repair of damage accrued during exposure to thermal extremes, or negative impacts from cumulative damage during successive exposures. We discuss the mechanisms underlying these differing effects. Fluctuating temperatures could be used to enhance or weaken insects in applied rearing programs, and any prediction of insect performance in the field—including models of climate change or population performance—mus...
552 citations
TL;DR: A physiological model is outlined that integrates several of the adaptation and acclimation responses that allow some insects to tolerate low temperatures and discusses how they collectively help to preserve cellular, organ, and organismal homeostasis at low temperature.
Abstract: Cold tolerance is important in defining the distribution of insects. Here, we review the principal physiological mechanisms underlying homeostatic failure during cold exposure in this diverse group of ectotherms. When insects are cooled sufficiently, they suffer an initial loss of neuromuscular function (chill coma) that is caused by decreased membrane potential and reduced excitability of the neuromuscular system. For chill-susceptible insects, chronic or severe chilling causes a disruption of ion and water homeostasis across membranes and epithelia that exacerbate the initial effects of chilling on membrane potential and cellular function, and these perturbations are tightly associated with the development of chill injury and mortality. The adaptation and acclimation responses that allow some insects to tolerate low temperatures are multifactorial and involve several physiological systems and biochemical adjustments. In this review, we outline a physiological model that integrates several of these respo...
274 citations
TL;DR: The 'tried and true' measures of insect cold tolerance, the equipment necessary for these measurement, and the ecological and biological significance of each are covered, and a framework and workflow for measuring cold tolerance and low temperature performance in insects is suggested.
260 citations
Cites background from "Physiological mechanisms of seasona..."
...Because the mechanisms of RCH are still poorly understood (Teets and Denlinger, 2013), it is not entirely clear whether these different treatments eliciting ‘RCH’ are actually triggering the same physiological response, so it is important to report the methods fully, and potentially include several different treatments in a study (e....
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...Because the mechanisms of RCH are still poorly understood (Teets and Denlinger, 2013), it is not entirely clear whether these different treatments eliciting ‘RCH’ are actually triggering the same physiological response, so it is important to report the methods fully, and potentially include several…...
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...Rapid cold-hardening (RCH) is the shortest time-scale of plastic responses, and describes enhanced survival of temperature extremes after a brief (minutes to c. 3 h) pre-exposure to sub-lethal temperatures (reviewed by Teets and Denlinger, 2013)....
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...RCH may be induced by slow cooling, diurnal cycles and mild low temperatures (usually 2 to þ4 °C) (Teets and Denlinger, 2013)....
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...…laboratory, and acclimatization, which happens in nature, although the mechanisms of acclimation and acclimatization are assumed to be similar (Kingsolver, 2009; Tattersall et al., 2012), but different to the mechanisms underlying hardening (Sinclair and Roberts, 2005; Teets and Denlinger, 2013)....
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TL;DR: The results are consistent with and extend the current understanding of the mechanisms of insect chilling tolerance, with proline and glutathione metabolism being the most strongly-supported metabolic pathways associated with increased cold tolerance.
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.
175 citations
TL;DR: Investigating D. suzukii phenology and seasonal adaptations can lead to a better understanding of the mechanisms through which insects express phenotypic plasticity, which likely enables invasive species to successfully colonize a wide range of environments.
Abstract: As global climate change and exponential human population growth intensifies pressure on agricultural systems, the need to effectively manage invasive insect pests is becoming increasingly important to global food security. Drosophila suzukii is an invasive pest that drastically expanded its global range in a very short time since 2008, spreading to most areas in North America and many countries in Europe and South America. Preliminary ecological modeling predicted a more restricted distribution and, for this reason, the invasion of D. suzukii to northern temperate regions is especially unexpected. Investigating D. suzukii phenology and seasonal adaptations can lead to a better understanding of the mechanisms through which insects express phenotypic plasticity, which likely enables invasive species to successfully colonize a wide range of environments. We describe seasonal phenotypic plasticity in field populations of D. suzukii. Specifically, we observed a trend of higher proportions of flies with the winter morph phenotype, characterized by darker pigmentation and longer wing length, as summer progresses to winter. A laboratory-simulated winter photoperiod and temperature (12:12 L:D and 10 °C) were sufficient to induce the winter morph phenotype in D. suzukii. This winter morph is associated with increased survival at 1 °C when compared to the summer morph, thus explaining the ability of D. suzukii to survive cold winters. We then used RNA sequencing to identify gene expression differences underlying seasonal differences in D. suzukii physiology. Winter morph gene expression is consistent with known mechanisms of cold-hardening such as adjustments to ion transport and up-regulation of carbohydrate metabolism. In addition, transcripts involved in oogenesis and DNA replication were down-regulated in the winter morph, providing the first molecular evidence of a reproductive diapause in D. suzukii. To date, D. suzukii cold resistance studies suggest that this species cannot overwinter in northern locations, e.g. Canada, even though they are established pests in these regions. Combining physiological investigations with RNA sequencing, we present potential mechanisms by which D. suzukii can overwinter in these regions. This work may contribute to more accurate population models that incorporate seasonal variation in physiological parameters, leading to development of better management strategies.
159 citations
Cites background from "Physiological mechanisms of seasona..."
...Inhibition of apoptotic cell death, MAP kinase signaling, and calcium signaling have all been found to be important mechanisms of the rapid cold-hardening response, but have not been found to occur in seasonal cold-hardening [19]....
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...There are two main classes of cold-hardening: (1) seasonal cold-hardening, which is induced over a timescale of days to weeks, and (2) rapid cold-hardening, which can occur in minutes or hours, and is induced by a sudden drop in temperature like a cold snap [19]....
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References
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TL;DR: Nonenzymatic mechanisms that impact MAP kinase functions and findings from gene disruption studies are highlighted and particular emphasis is on ERK1/2.
Abstract: Mitogen-activated protein (MAP) kinases comprise a family of ubiquitous proline-directed, protein-serine/threonine kinases, which participate in signal transduction pathways that control intracellular events including acute responses to hormones and major developmental changes in organisms. MAP kinases lie in protein kinase cascades. This review discusses the regulation and functions of mammalian MAP kinases. Nonenzymatic mechanisms that impact MAP kinase functions and findings from gene disruption studies are highlighted. Particular emphasis is on ERK1/2.
4,040 citations
TL;DR: This work discloses that expression of Hsps can occur in nature, all species have hsp genes but they vary in the patterns of their expression, and Hsp expression can be correlated with resistance to stress, and species' thresholds for HSP expression are correlated with levels of stress that they naturally undergo.
Abstract: Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
3,841 citations
01 Jun 1999
TL;DR: This review of recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction concludes that cold acclimation includes the expression of certain cold-induced genes that function to stabilize membranes against freeze-induced injury.
Abstract: ▪ Abstract Many plants increase in freezing tolerance upon exposure to low nonfreezing temperatures, a phenomenon known as cold acclimation. In this review, recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction are described. One of the important conclusions to emerge from these studies is that cold acclimation includes the expression of certain cold-induced genes that function to stabilize membranes against freeze-induced injury. In addition, a family of Arabidopsis transcription factors, the CBF/DREB1 proteins, have been identified that control the expression of a regulon of cold-induced genes that increase plant freezing tolerance. These results along with many of the others summarized here further our understanding of the basic mechanisms that plants have evolved to survive freezing temperatures. In addition, the findings have potential practical applications as freezing te...
2,938 citations
"Physiological mechanisms of seasona..." refers background in this paper
...Cold acclimation in plants, which occurs in the order of days to weeks (Thomashow, 1999), is calcium-regulated, and it is hypothesized that calcium similarly governs rapid responses to low temperature in insects....
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01 Jan 1999
TL;DR: A review of recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction are described in this article.
Abstract: ▪ Abstract Many plants increase in freezing tolerance upon exposure to low nonfreezing temperatures, a phenomenon known as cold acclimation. In this review, recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction are described. One of the important conclusions to emerge from these studies is that cold acclimation includes the expression of certain cold-induced genes that function to stabilize membranes against freeze-induced injury. In addition, a family of Arabidopsis transcription factors, the CBF/DREB1 proteins, have been identified that control the expression of a regulon of cold-induced genes that increase plant freezing tolerance. These results along with many of the others summarized here further our understanding of the basic mechanisms that plants have evolved to survive freezing temperatures. In addition, the findings have potential practical applications as freezing te...
2,665 citations
TL;DR: The acquisition of the biochemical and ultrastructural features of apoptosis critically relies on the liberation of apoptogenic proteases or protease activators from mitochondria.
Abstract: Both physiological cell death (apoptosis) and, in some cases, accidental cell death (necrosis) involve a two-step process. At a first level, numerous physiological and some pathological stimuli trigger an increase in mitochondrial membrane permeability. The mitochondria release apoptogenic factors through the outer membrane and dissipate the electrochemical gradient of the inner membrane. Mitochondrial permeability transition (PT) involves a dynamic multiprotein complex formed in the contact site between the inner and outer mitochondrial membranes. The PT complex can function as a sensor for stress and damage, as well as for certain signals connected to receptors. Inhibition of PT by pharmacological intervention on mitochondrial structures or mitochondrial expression of the apoptosis-inhibitory oncoprotein Bcl-2 prevents cell death, suggesting that PT is a rate-limiting event of the death process. At a second level, the consequences of mitochondrial dysfunction (collapse of the mitochondrial inner transmembrane potential, uncoupling of the respiratory chain, hyperproduction of superoxide anions, disruption of mitochondrial biogenesis, outflow of matrix calcium and glutathione, and release of soluble intermembrane proteins) entails a bioenergetic catastrophe culminating in the disruption of plasma membrane integrity (necrosis) and/or the activation of specific apoptogenic proteases (caspases) by mitochondrial proteins that leak into the cytosol (cytochrome c, apoptosis-inducing factor) with secondary endonuclease activation (apoptosis). The relative rate of these two processes (bioenergetic catastrophe versus protease and endonuclease activation) determines whether a cell will undergo primary necrosis or apoptosis. The acquisition of the biochemical and ultrastructural features of apoptosis critically relies on the liberation of apoptogenic proteases or protease activators from mitochondria. The fact that mitochondrial events control cell death has major implications for the development of cytoprotective and cytotoxic drugs.
2,034 citations
"Physiological mechanisms of seasona..." refers background in this paper
...Although the underlying mechanisms of cold-induced apoptosis are unknown, it may be a consequence of calcium imbalance and mitochondrial malfunction, both of which are known to trigger apoptosis in a range of animal systems (Kroemer et al ., 1998)....
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...Initially, these results appeared counterintuitive because apoptosis is considered to be a protective mechanism that safely eliminates damaged cells (Kroemer et al ., 1998)....
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