Cryobiology of the freeze-tolerant gall fly Eurosta solidaginis: overwintering energetics and heat shock proteins

Lee, Richard; Dommel, Robyn A; Joplin, Karl H.; Denlinger, David L.

doi:10.3354/cr005061

Cited by 36 publications

(32 citation statements)

References 14 publications

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“…By late November, larval mass had decreased by approximately 10·mg, which is consistent with previous reports for this species (Lee et al, 1995;Rojas et al, 1986). The decrease in body mass is associated with the relatively higher environmental temperatures, and thus, higher metabolic and lipid utilization rates in late autumn compared to midwinter (Lee et al, 1995;Irwin and Lee, 2003).…”

Section: Discussionsupporting

confidence: 90%

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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Section: Discussionsupporting

confidence: 90%

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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“…The biology of E. solidaginis has been investigated for many decades (Collins et al, 1997;Lee et al, 1995;Salt, 1959;Williams et al, 2004) and therefore it is surprising that this is the first report of these abundant acTAGs. We suspect that this oversight arises because the techniques for studying lipids (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…Over winter, E. solidaginis pre-pupae are freeze tolerant, and their cold hardiness has been investigated for over 50 years (Collins et al, 1997;Lee et al, 1995;Salt, 1959). Eurosta solidaginis pre-pupae remodel their membrane phospholipids and lcTAGs in preparation for winter, resulting in increased membrane fluidity at low temperatures via increased abundance of unsaturated fatty acids and phosphatidylcholine (Bennett et al, 1997;Pruitt and Lu, 2008).…”

Section: Research Articlementioning

confidence: 99%

Seasonal accumulation of acetylated triacylglycerols by a freeze-tolerant insect

Marshall

Thomas

Roxin

et al. 2014

Journal of Experimental Biology

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Most animals store energy as long-chain triacylglycerols (lcTAGs). Trace amounts of acetylated triacylglycerols (acTAGs) have been reported in animals, but are not accumulated, likely because they have lower energy density than lcTAGs. Here we report that acTAGs comprise 36% of the neutral lipid pool of overwintering prepupae of the goldenrod gall fly, Eurosta solidaginis, while only 17% of the neutral lipid pool is made up of typical lcTAGs. These high concentrations of acTAGs, present only during winter, appear to be synthesized by E. solidaginis and are not found in other freezetolerant insects, nor in the plant host. The mixture of acTAGs found in E. solidaginis has a significantly lower melting point than equivalent lcTAGs, and thus remains liquid at temperatures at which E. solidaginis is frozen in the field, and depresses the melting point of aqueous solutions in a manner unusual for neutral lipids. We note that accumulation of acTAGs coincides with preparation for overwintering and the seasonal acquisition of freeze tolerance. This is the first observation of accumulation of acTAGs by an animal, and the first evidence of dynamic interconversion between acTAGs and lcTAGs during development and in response to stress. INTRODUCTIONLipids fulfill diverse biological functions including cell membrane structure, signalling and energy storage (Canavoso et al., 2001;Reue, 2011;Yen et al., 2008). Long-chain triacylglycerols (lcTAGs) are generally used as fuel stores by animals because of their high energy density, and are consequently the most abundant lipid class in animals (Williams et al., 2011;Yen et al., 2008). No other neutral lipid has been reported as a storage molecule in terrestrial animals.Instead of having three long-chain fatty esters (as in lcTAGs), acetylated triacylglycerols (acTAGs) have an acetyl group esterified at the 3-position of the glycerol backbone. This distinct structure results in the reduced viscosity and the significantly lower energy density of acTAGs compared with lcTAGs (Durrett et al., 2010). Trace amounts of acTAGs have been described in a broad range of organisms, including the antlers of Japanese deer (Cervus nippon) (Yang et al., 2004), the udders of domestic cows (Bos primigenius) (Limb et al., 1999) and the seeds of the burning bush plant (Euonymus alatus) (Durrett et al., 2010). acTAGs constitute a very small proportion of the total lipid pool in the two mammal species investigated [<0.1% by mass Limb et al., 1999;Yang et al., 2004)], but predominate (92% by moles) in E. alatus seed oils (Durrett et al., 2010). Euonymus alatus synthesises acTAGs via an unusual diacylglycerol acyltransferase (DGAT) by esterifying an acetyl group, rather than a third long-chain fatty acid, to diacylglycerol (DAG) (Durrett et al., 2010). Although trace acTAGs are present in a few animals, we are not aware of any clear hypotheses for a physiological role of acTAGs in biological systems. Here we report that the goldenrod gall fly, Eurosta solidaginis (Fitch 1855), accumulates significan...

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“…For example, the cold hardiness of the freeze tol erant Eurosta solidaginis (Diptera: Tephritidae) is related to the latitude of origin (Lee et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

Cold hardiness of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) from central and southern Europe

Kalushkov¹,

Nedvěd²

2000

Eur. J. Entomol.

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Abstract. The cold hardiness of individuals from overwintering populations of a freeze susceptible bug Pyrrhocoris apterus from central and southern Europe differed significantly. Supercooling point (SCP) correlated well with both lethal temperature (LT50) and lethal time (Lt50), and is a good index of cold hardiness of adults during and after diapause. In January, diapause terminated, but cold hardiness was similar to that recorded in November; cold hardiness decreased slightly in March and markedly in May. Short expo sure (less than a week) to higher temperatures before termination of diapause did not reduce the cold hardiness. Cold hardiness did not closely follow air temperatures.The Bulgarian bugs retained lower cold hardiness regardless of acclimation to harsh field condi tions in the Czech Republic. The interpopulation difference is therefore a heritable character representing an adjustment to local cli mates.

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Cryobiology of the freeze-tolerant gall fly Eurosta solidaginis: overwintering energetics and heat shock proteins

Cited by 36 publications

References 14 publications

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

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

Seasonal accumulation of acetylated triacylglycerols by a freeze-tolerant insect

Cold hardiness of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) from central and southern Europe

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