The large cabbage white, Pieris brassicae (L.), is a pest of Brassicaceae family which overwinters as a pupa on different host plants or other shelters. Little information is available on the physiological changes during overwintering of this pest and its cold tolerance. In the current study, the cryoprotectants were identified by LC/MS and their changes were examined by HPLC in specimens collected during the months of autumn and winter, as well as lab-reared pupae which treated one week at 27, 15, 10, 7, and 4 °C. The changes of glycogen content were investigated as the main source of cryoprotectants. Four compounds of trehalose, sorbitol, glucose, and inositol were identified and trehalose and sorbitol showed the highest increase in the winter months and these changes were accompanied by a significant decrease in the glycogen content. In lab-reared pupae treated in 7 and 4 °C, trehalose and sorbitol significantly increased. Therefore, it seems that trehalose and sorbitol, as the most important cryoprotectants, play a significant role in tolerating of low temperatures of winter and tolerating temperatures below 10 °C can induce the production of such compounds in this species.
Araghieh Farahani, F., Moharramipour, S. & Fathipour, Y. (2014). Changes of low molecular weight compounds of cryoprotectants in overwintering adults of Eurygaster integriceps (Hem.: Scutelleridae). Journal Entomological of Society of Iran, 34(1), 23-34.
Atapour, M. & Moharramipour, S. (2009). Changes in supercooling point and glycogen reserves in overwintering and lab-reared samples of beet armyworm, Spodoptera exigua (Lep.: Noctuidae) to determining of cold hardiness strategy.Entomology and Phytopathology, 78(2), 199-216.
Atapour, M. & Moharramipour, S. (2009). Changes of cold hardiness, supercooling capacity, and major cryoprotectants in overwintering larvae of Chilo suppressalis (Lepidoptera: Pyralidae). Environmental Entomology, 38, 260-265.
Atapour, M. (2016). Overwintering and Cold Tolerance in Pupae of Large Cabbage White, Pieris brassicae (Lepidoptera: Pieridae) in Iran. Iranian Journal of Plant Production Science In Press. (in Farsi)
Bale, J. S. (2002). Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London, 357(B), 849-862.
Bale, J. S., Hansen, T. N., Nishino, M. & Baust, J. G. (1989). Effect of cooling rate on the survival of larvae, pupariation, and adult emergence of the gallfly Eurosta solidaginis. Cryobiology, 2, 285-289.
Baust, J. G. & Rojas, R. R. (1985). Review. Insect cold hardiness: facts and fancy. Journal of Insect Physiology, 31, 755-759.
Chino, H. (1957). Conversion of glycogen into sorbitol and glycerol in the diapausing eggs of Bombyx silkworm. Nature, 180, 606-607.
Chown, S. L. & Sinclair, B. J. (2010). The macrophysiology of insect cold-hardiness. In: D. L. Denlinger and R. E. Lee, eds. Low Temperature Biology of Insects. Cambridge University Press. pp. 191-222.
Crowe, L. M. (2002). Lessons from nature: the role of sugars in anhydrobiosis. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology, 131, 505-513.
Danilevskii, A. S. (1965). Photoperiodism and seasonal development of insects. Oliver and Boyd, Edinburg. 283 pages.
Danks, H. V. (2000). Dehydration in dormant insects. Journal of Insect Physiology, 46, 837-852.
Denlinger, D. L. (1991). Relationship between cold hardiness and diapause, In: R. E. Lee and D. L. Denlinger, (Eds.) Insect at Low Temperature. Chapman and Hall, New York. pp. 174-198.
Denlinger, D. L. (2002). Regulation of diapause. Annual Review of Entomology, 47, 93-122.
Ding, L., Li, Y. & Goto, M. (2003). Physiological and biochemical changes in summer and winter diapause and non-diapause pupae of the cabbage armyworm, Mamestra brassacae L. during long-term cold acclimation. Journal of Insect Physiology, 49, 1153-1159.
Duman, J. G., Neven, L. G., Beals, J. M., Olson, K. O. & Castellino, F. J. (1985). Freeze tolerance adaptations, including haemolymph protein and lipoprotein ice nucleators, in larvae of the cranefly Tipula trivittata. Journal of Insect Physiology, 31, 1-9.
Folch, J., Lees, M. & Sloane-Stanley, GH. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497-509.
Goto, M., Fujii, M., Suzuki, K. & Sakai, M. (1998). Factors affecting carbohydrate and free amino acid content in overwintering larvae of Enosima leucotaeniella. Journal of Insect Physiology, 44, 87-94.
Hamedi, N., Moharramipour, S. & Barzegar, M. (2013). Temperature dependent chemical components accumulation in Hippodamia variegata (Coleoptera: Coccinellidae) during overwintering. Environmental Entomology, 42(2), 375-80.
Hansen, R. G., Rutter, W. J. & Craine, E. M. (1951). A nephelometric method for the determination of glycogen. Journal of Biological Chemistry, 195, 127-132.
Hilal, A. (1977). Mise en evidence d’un etat de diapause vraie chez Sesamia nonagrioides Lef. (Lepidoptera-Noctuidae). Comptes Rendus de l'Académie des Sciences Paris. Ser. D, 365, 367-285.
Horwath, K. L. & Duman, J. G. (1984). Further studies on the involvement of the circadian system in photoperiodic control of antifreeze protein production in the beetle Dendroides canadensis. Journal of Insect Physiology, 30, 947-955.
Jõgar, K., Metspalu, L., Hiiesaar, K., Luik, A., Martin, A.-J., Mänd, M., Jaaniso, R. & Kuusik, A. (2005). Physiology of diapause in pupae of Pieris brassicae L. (Lepidoptera: Pieridae). Agronomy Research, 3(1), 21-37.
Khani, A., Moharramipour, S. & Barzegar, M. (2007). Cold tolerance and trehalose accumulation in overwintering larvae of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). European Journal of Entomology, 104, 385-392.
Khanjani, M. (2006). Vegetable pests in Iran. Bu-Ali Sina University Publication, 2nd Edition. 467 pp. (in Farsi)
Kostal, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52, 113-127.
Kostal, V., Slachta, M. & Simek, P. (2001). Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comparative Biochemistry and Physiology, 130(B), 365-374.
Kostal, V., Zahradnickova, H., Simek, P. & Zeleny, J. (2007). Multiple component system of sugars and polyols in the overwintering spruce bark beetle, Ips typographus. Journal of Insect Physiology, 53, 580-586.
Lee, K., Chang, Y. & Kim, Y. (2002). Trehalose, a major cryoprotectant of the overwintering rice water weevil, Lissorhoptrus oryzophilus (Coleoptera: Curculionidae). Journal of Asia-Pacific Entomology, 5, 35-41.
Lee, R. E. (2010). A primer on insect cold-tolerance. In: D. L. Denlinger, and R. E. Lee, (Eds). Low Temperature Biology of Insects. 390 pp. Cambridge University Press. pp. 3-34.
Li, Y. P., Goto, M., Ito, S., Sato, Y., Sasaki, K. & Goto, N. (2001). Physiology of diapause and cold hardiness in the overwintering pupae of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae) in Japan. Journal of Insect Physiology, 47, 1181-1187.
Li, Y. P., Goto, M., Ito, S., Sato, Y., Sasaki, K. & Goto, N. (2001). Physiology of diapause and cold hardiness in the overwintering pupae of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae) in Japan. Journal of Insect Physiology, 47, 1181-1187.
Moreau, R., Olivier, D., Gourdoux, L. & Dutrieu, J. (1981). Carbohydrate metabolism in Pieris brassicae L. (Lepidoptera); variations during normal and diapausing development. Comparative Biochemistry and Physiology. A, Comparative Physiology, 68(B), 95-99.
Naeemullah, M. & Takeda, M. (1998). Selection for fast and slow development rates affected diapause and other developmental traits in Plodia interpunctella (Lepidoptera: Phycitidae). Entomological Science, 1, 503-510.
Pullin, A. S. & Bale, J. S. (1989a). Effects of low temperature on diapausing Aglais urticae and Inachis io (Lepidoptera: Nymphalidae): cold hardiness and overwintering survival. Journal of Insect Physiology, 35, 277-281.
Pullin, A. S. & Bale, J. S. (1989b). Influence of diapause and temperature on cryoprotectant synthesis and cold hardiness in pupae of Pieris brassicae. Comparative Biochemistry and Physiology. A, Comparative Physiology, 94, 499-503.
Pullin, A. S., Bale, J. S. & Fontaine, X. L. R. (1991). Physiological aspects of diapause and cold tolerance during overwintering in Pieris brassicae. Physiological Entomology, 16, 447-456.
Saeidi, F., Moharramipour, S. & Barzegar, M. (2012). Seasonal patterns of cold hardiness and cryoprotectant profiles in Brevicoryne brassicae (Hemiptera: Aphididae). Environmental Entomology, 41, 1638-1643.
Salt, R. W. (1961). Principles of insect cold-hardiness. Annual Review of Entomology, 6, 55-74.
Soudi, S. & Moharramipour, S. (2012). Seasonal patterns of the thermal response in relation to sugar and polyol accumulation in overwintering adults of elm leaf beetle, Xanthogaleruca luteola (Coleoptera: Chrysomelidae). Journal of Thermal Biology, 37, 384-391.
Storey, K. B. & Storey, J. M. (1988). Freeze tolerance in animals. Physiological Reviews, 68, 27-84.
Storey, K. B. & Storey, J. M. (1991). Biochemistry of cryoprotectants. In: Lee, R. E. and D. L. Denlinger, (Eds.) Insect at Low Temperature. New York, Chapman and Hall. pp. 64-93.
Worland, M. R., Grubor-Lajsic, G., & Montiel, P. O. (1998). Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology, 44, 211-219.
Worland, M. R., Leinaas, H. P. & Chown, S. L. (2006). Supercooling point frequency distributions in Collembola are affected by moulting. Functional Ecology, 20, 323-329.
Zachariassen, K. E. (1985). Physiology of cold tolerance in insects. Physiological Reviews, 65, 799-832.
Atapour, M. (2017). Cryoprotectants in lab-reared and overwintering pupae of large cabbage white, Pieris brassicae (Lepidoptera: Pieridae). Iranian Journal of Plant Protection Science, 48(1), 139-150. doi: 10.22059/ijpps.2017.204400.1006705
MLA
Maryam Atapour. "Cryoprotectants in lab-reared and overwintering pupae of large cabbage white, Pieris brassicae (Lepidoptera: Pieridae)", Iranian Journal of Plant Protection Science, 48, 1, 2017, 139-150. doi: 10.22059/ijpps.2017.204400.1006705
HARVARD
Atapour, M. (2017). 'Cryoprotectants in lab-reared and overwintering pupae of large cabbage white, Pieris brassicae (Lepidoptera: Pieridae)', Iranian Journal of Plant Protection Science, 48(1), pp. 139-150. doi: 10.22059/ijpps.2017.204400.1006705
VANCOUVER
Atapour, M. Cryoprotectants in lab-reared and overwintering pupae of large cabbage white, Pieris brassicae (Lepidoptera: Pieridae). Iranian Journal of Plant Protection Science, 2017; 48(1): 139-150. doi: 10.22059/ijpps.2017.204400.1006705