Seasonal changes in the composition of storage and membrane lipids in overwintering larvae of the codling moth, Cydia pomonella

Abstract

The codling moth (Cydia pomonella) is a major insect pest of apples worldwide. It overwinters as a diapausing fifth instar larva. The overwintering is often a critical part of the insect life-cycle in temperate zone. This study brings detailed analysis of seasonal changes in lipid composition and fluidity in overwintering larvae sampled in the field. Fatty acid composition of triacylglycerol (TG) depots in the fat body and relative proportions of phospholipid (PL) molecular species in biological membranes were analyzed. In addition, temperature of melting (Tm) in TG depots was assessed by using differential scanning calorimetry and the conformational order (fluidity) of PL membranes was analyzed by measuring the anisotropy of fluorescence polarization of diphenylhexatriene probe in membrane vesicles. We observed a significant increase of relative proportion of linoleic acid (C18:2n6) at the expense of palmitic acid (C16:0) in TG depots during the larval transition to diapause accompanied with decreasing melting temperature of total lipids, which might increase the accessibility of depot fats for enzymatic breakdown during overwintering. The fluidity of membranes was maintained very high irrespective of developmental mode or seasonally changing acclimation status of larvae. The seasonal changes in PL composition were relatively small. We discuss these results in light of alternative survival strategies of codling moth larvae (supercooling vs. freezing), variability and low predictability of environmental conditions, and other cold tolerance mechanisms such as extending the supercooling capacity and massive accumulation of cryoprotective metabolites.

Diapause induces remodeling of the fatty acid composition of membrane and storage lipids in overwintering larvae of Ostrinia nubilalis, Hubn. (Lepidoptera: Crambidae)

“…The FA composition of lipids has been thoroughly analyzed in many insects to understand the dynamic and complex physiological state of diapause (Spike et al, 1991;Ohtsu et al, 1993;Koštál et al, 2003;Basham and Cakmak, 2005;Michaud and Denlinger, 2006;Khani et al, 2007;Koštál, 2010;Rozsypal et al, 2014). The FA composition of triacylglycerols and phospholipids extracted from the whole bodies of non-diapausing and (Fast, 1970;Thompson 1973;Atapour et al, 2007;Khani et al, 2007).…”

“…In this study on O. nubilalis, palmitoleic acid (16:1n-7) comprise a prominent proportion of the total FAs in triacylglycerol and phospholipid FA pools, which is unusual for a Lepidopteran species but more characteristic of Dipteran species (Fast, 1970;Thompson 1973;Buckner et al, 2004). Many authors have found that changes in the FA composition of triacylglycerols and phospholipids are strongly associated with a physiological state of diapause during which many insects develop cold hardiness (Bennet et al, 1997;Kostal and Simek, 1998;Koštál et al, 2003;Buckner et al, 2004;Bashan and Cakmak, 2005;Michaud and Denlinger, 2006;Rozsypal et al, 2014). In O. nubilalis, changes in the FA composition of triacylglycerols and phospholipids led to a significant increase in the overall FA unsaturation (UFAs/SFAs ratio) during transition and time course of diapause, which significantly decreased during the termination period.…”

“…Also, MUFAs, due to the central position of the double bond in FA, maximize the lateral displacement of the end of the chain and contribute to overall membrane disorder (Barton and Gunston, 1975). Thus, high levels of cis oleic acid The seasonal increase in overall FA unsaturation of storage and membrane lipids is considered to be an adaptation to optimize phase behaviour that is crucial for controlling membrane fluidity and storage utilization during low winter temperatures (Sinesky, 1974;Hazel, 1989;Hazel, 1995;Hazel and Williams, 1990;Ohtsu et al, 1993;Kostal and Simek, 1998;Hochachka and Somero, 2002;Koštál et al, 2003;Michaud and Denlinger, 2006;Overgaard et al, 2008;Van Dooremalen and Ellers, 2010;Rozsypal et al, 2014). Namely, increased FA unsaturation of membrane phospholipids contributes to the maintenance of the vital static order and dynamic properties of membranes whereas triacylglycerols maintain the fluidity of storage lipids facilitating accessibility of enzymes to energy lipid reserves during periods of low winter temperatures.…”

“…12 metabolized by lipases as those in a liquid phase (Sinesky, 1974;Ohtsu et al, 1993;Hazel, 1987;Hazel, 1995;Joanisse and Storey, 1996;Bennet et al, 1997;Kostal and Simek, 1998;Buckner et al, 2004;Atapour et al, 2007;Van Dooremalen et al, 2011;Rozsypal et al, 2014).…”

The many roles of fats in overwintering insects

“…For example, both E. solidaginis and E. scudderiana have more unsaturated lipids in winter than in summer (Joanisse and Storey, 1996) and, as a consequence of this, E. solidaginis has lipid droplets that remain sufficiently liquid to coalesce when the cytoplasm of the cell freezes (Salt, 1959;Lee et al, 1993). Similarly, the proportion of polyunsaturated (18:2) fatty acids in the storage lipids of codling moth (Cydia pomonella) larvae increases during winter, with a consequent 5-10°C decrease in the melting point of the storage lipids (Rozsypal et al, 2015). Although vertebrates generally cannot synthesise polyunsaturated fatty acids (PUFAs), or desaturate monounsaturated fatty acids to generate PUFAs, several groups of insects (notably excluding Drosophila) appear able to do so (de Renobales et al, 1987;Stanley-Samuelson et al, 1988).…”