Insect cold-hardiness and ice nucleating active microorganisms including their potential use for biological control

Lee, Richard; Lee, Marcia R.; Strong‐Gunderson, Janet M.

doi:10.1016/0022-1910(93)90011-f

Cited by 76 publications

(56 citation statements)

References 89 publications

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“…Understanding the mechanisms by which insects tolerate low temperature is essential for predicting their response to a changing climate (53). Furthermore, mechanisms of cold hardening can be exploited to manipulate populations of insect pests (54). Our group has recently explored the possibility of disrupting overwintering diapause to control pest populations (55), and we envision disruption of acute cold hardening to be an equally effective strategy.…”

Section: Resultsmentioning

confidence: 99%

Calcium signaling mediates cold sensing in insect tissues

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Lee

et al. 2013

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

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The ability to rapidly respond to changes in temperature is a critical adaptation for insects and other ectotherms living in thermally variable environments. In a process called rapid cold hardening (RCH), insects significantly enhance cold tolerance following brief (i.e., minutes to hours) exposure to nonlethal chilling. Although the ecological relevance of RCH is well-established, the underlying physiological mechanisms that trigger RCH are poorly understood. RCH can be elicited in isolated tissues ex vivo, suggesting coldsensing and downstream hardening pathways are governed by brain-independent signaling mechanisms. We previously provided preliminary evidence that calcium is involved in RCH, and here we firmly establish that calcium signaling mediates cold sensing in insect tissues. In tracheal cells of the freeze-tolerant goldenrod gall fly, Eurosta solidaginis, chilling to 0°C evoked a 40% increase in intracellular calcium concentration as determined by live-cell confocal imaging. Downstream of calcium entry, RCH conditions significantly increased the activity of calcium/calmodulin-dependent protein kinase II (CaMKII) while reducing phosphorylation of the inhibitory Thr306 residue. Pharmacological inhibitors of calcium entry, calmodulin activation, and CaMKII activity all prevented ex vivo RCH in midgut and salivary gland tissues, indicating that calcium signaling is required for RCH to occur. Similar results were obtained for a freeze-intolerant species, adults of the flesh fly, Sarcophaga bullata, suggesting that calcium-mediated cold sensing is a general feature of insects. Our results imply that insect tissues use calcium signaling to instantly detect decreases in temperature and trigger downstream cold-hardening mechanisms.ow temperature is one of the primary constraints for insects and other ectotherms living in temperate and polar regions (1). Although seasonal adaptations to cold stress, including environmentally programmed periods of dormancy called diapause, have been well-studied (2-5), physiological responses to sudden changes in temperature have received less attention. In a process termed rapid cold hardening (RCH), insects dramatically enhance their cold tolerance in a matter of minutes to hours (6). For example, in the flesh fly, Sarcophaga crassipalpis, the first species in which RCH was described, exposure to 0°C for as little as 30 min significantly enhances cold tolerance at −10°C (6). RCH has since been described in dozens of insect species (7), including both freeze-intolerant (insects in which internal ice formation is lethal) and freeze-tolerant species (insects that tolerate internal ice formation) (8, 9). Naturally occurring thermoperiods can elicit RCH (10), and RCH preserves essential functions such as courtship and mating (11,12), supporting the relevance of this process to natural populations.Although the ecological relevance of RCH has been established, the physiological mechanisms are poorly understood. RCH results in a slight increase in the cryoprotectant glycerol (6, 13),...

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Section: Resultsmentioning

confidence: 99%

Calcium signaling mediates cold sensing in insect tissues

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Lee

et al. 2013

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

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“…Death at cellular levels does not always correlate with organismal mortality (Yi and Lee, 2003). Previously, we reported that fat body survived freezing at significantly lower temperatures than did the intact E. solidaginis larvae (Lee et al, 1993). Using fluorescent vital dyes to assess tissue viability in these larvae, Yi and Lee (2003) found that integumentary muscle, hemocytes, trachea, MT, fat body and gut were more tolerant of freezing than the whole animal.…”

Section: Of Gut and Malpighian Tubulementioning

confidence: 98%

“…Fully cold-hardened larvae are freeze-tolerant and survive freezing at -25°C with 75% reaching adulthood (Lee et al, 1993). In the present study, we used larval responsiveness to tactile stimuli as the criterion of survival.…”

Section: Of Gut and Malpighian Tubulementioning

confidence: 99%

“…The goldenrod gall fly Eurosta solidaginis is a naturally freeze-tolerant insect that survives both intra-(as in the case of fat body cells) and extra-cellular (Salt, 1959;Lee et al, 1993;Bennett and Lee, 1997) freezing. During autumn, third instar larvae increase their cold-hardiness and become tolerant of extensive internal ice formation, partly owing to the accumulation of the cryoprotectants glycerol, sorbitol and trehalose (Baust and Lee, 1981;Lee and Hankison, 2003).…”

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Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall flyEurosta solidaginis

Lee

2005

Journal of Experimental Biology

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SUMMARY Since few studies have examined cold tolerance at the organ level in insects, our primary objective was to characterize the functional responses of the gut and Malpighian tubules (MT) to seasonal acclimatization, chilling and freezing in larvae of the goldenrod gall fly Eurosta solidaginisFitch (Diptera, Tephritidae). From September to December, hemolymph osmolality(455-926 mOsmol kg l-1) and freezing tolerance increased markedly in field-collected larvae. Chlorophenol Red was readily transported into the lumen of the foregut, the posterior portion of the midgut, the ureter, the proximal region of the anterior pair of MT, and entire posterior pair of MT. Ouabain and KCN inhibited transport of Chlorophenol Red in the gut and MT. Transport was readily detected at 0°C and the rate of transport was directly related to temperature. The rate of fluid transport by the MT decreased steadily from a monthly high in September (10.7±0.8 nl min-1 for the anterior pair; 12.7±1.0 nl min-1for the posterior pair) until secretion was no longer detectable in December;this decrease parallels entry into diapause for this species. Even in larvae that died following freezing for 40 days at -20°C, individual organ function was retained to a limited extent. Through the autumn, cholesterol concentrations in the hemolymph increased nearly fourfold. In contrast, the ratio of cholesterol to protein content (nmol mg l-1) in the MT membrane remained relatively constant (22∼24 nmol mg l-1protein) during this period. Freezing of larvae for 20 days at -20°C caused a significant decrease in cholesterol levels in the hemolymph and the MT membranes compared to unfrozen controls. These results suggest that cholesterol plays a role in seasonal cold hardening and freeze tolerance in insects.

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“…It might be expected therefore that such micro-organisms would form part of the natural flora of the digestive system of herbivorous and detritivorous insects and their predators, and this has now been confirmed for both bacteria and fungi in a range of insect species (Lee et al 1993b). It has also been suggested that these intestinal micro-organisms may act as INA in freeze-tolerant insects in which they have been found, such as Chilo suppressalis (Tsumuki et al 1992) and H. sparsutum (Worland & Block 1999).…”

Section: (C) Establishment Of Invasive Speciesmentioning

confidence: 99%

Insects and low temperatures: from molecular biology to distributions and abundance

Bale

2002

Phil. Trans. R. Soc. Lond. B

438

329

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Insects are the most diverse fauna on earth, with different species occupying a range of terrestrial and aquatic habitats from the tropics to the poles. Species inhabiting extreme low-temperature environments must either tolerate or avoid freezing to survive. While much is now known about the synthesis, biochemistry and function of the main groups of cryoprotectants involved in the seasonal processes of acclimatization and winter cold hardiness (ice-nucleating agents, polyols and antifreeze proteins), studies on the structural biology of these compounds have been more limited.The recent discovery of rapid cold-hardening, ice-interface desiccation and the daily resetting of critical thermal thresholds affecting mortality and mobility have emphasized the role of temperature as the most important abiotic factor, acting through physiological processes to determine ecological outcomes. These relationships are seen in key areas such as species responses to climate warming, forecasting systems for pest outbreaks and the establishment potential of alien species in new environments.

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Insect cold-hardiness and ice nucleating active microorganisms including their potential use for biological control

Cited by 76 publications

References 89 publications

Calcium signaling mediates cold sensing in insect tissues

Calcium signaling mediates cold sensing in insect tissues

Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall flyEurosta solidaginis

Insects and low temperatures: from molecular biology to distributions and abundance

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