Impact of photoperiod on circadian trehalose and trehalase rhythms in the digestive system of silkworm, Bombyx mori
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Abstract
Circadian trehalose and trehalase rhythms were studied in the digestive system of Bombyx mori under 12 hr light-dark cycle (LD), continuous light (LL) and continuous dark (DD). The rhythmic changes were interpreted as synthetic cycles in gut wall and release cycles in gut lumen. The trehalose rhythm of gut wall comprised 8 trehalose synthetic cycles (TS cycles) under LD and LL and 7 under DD. The 24 hr trehalose rhythm of LD and LL was clock shifted to 27.2 hr under DD. The trehalose rhythm included 4 TR cycles under LD, 5 under LL and DD in the gut lumen and the 24 hr rhythm of LD was clock shifted to 19.2 hr under LL and DD. In the gut wall trehalase rhythm maintained 8 trehalase enzyme synthetic cycles (TES cycles) under LD, 10 LL and 7 under DD and the 24 hr rhythm of LD was clock shifted to 19.2 hr under LL and 27.2 hr under DD. In the gut lumen it included 4 TER cycles under LD and DD, 5 under LL and its 24-hr rhythm was advanced to 19.2 hr. Further analysis of data showed that LD favours trehalose synthesis, while LL and DD favour trehalase synthesis.
Article Details
Article Details
Bombyx mori, Circadian trehalose rhythm, Circadian trehalase rhythm, Digestive system, Photoperiod
Anand, A .A. P., Vennison, S. J., Sankar, S.G., Prabhu, D.I.G., Vasan, P .T., Raghuraman,T., Geoffrey, C. J., Vendan, S. E. (2010). Isolation and characterization of bacteria from the gut of Bombyx mori that degrade Cellulose, xylan, pectin and starch and their impact on digestion. J. Insect. Sci., 10:107.
Azuma, M. and Yamashita, O. (1985). Cellular localization and proposed function of midgut trehalase in the silkworm larva, Bombyx mori. Tissue and Cell, 17: 539-551.
Banaroudj, N., Lee. D.H. and Goldberg, A.L. (2001). Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J.Biol.Chem., 276: 24261-24267.
Becker, A., Schloder, P., Steele, J.E. and Wegener, G. (1996). The regulation of trehlose metabolism in insects. Experientia., 52: 433-439.
Behroozi, E. (2010). Study on the nutritional reserves and cold hardiness of over wintering larvae of pistachio white leaf borer, Ocneria terebintina (Lepidoptera: lymantriidae) in Rafsanjan township and physiological evaluation of some IGRs against the larvae. M.Sc. thesis. Vali-e-A sr University of Raf Sanjan, Iran.
Bhuvaneswari, E. and Sivaprasad, S. (2012). Impact of photoperiod on circadian protein and protease rhythms in the digestive system of Silkworm, Bombyx mori. The Bioscan, 7: 175-183.
Bolat, I. (2008). The importance of trehalose in brewing yeast survival. Innovative Romanian food Biotechnology, 2: 1-10.
Candy, D.J. and Kilby, B. A. (1961). The biosynthesis of trehalose in the locust fatbody. Biochem. J., 78: 531-536.
Dahlman, D.L. (1971). Purification and properties of trehalase from tobacco hornworm larvae. J.Insect.Physiol., 17:1677-1689.
Egorova, T.A. and Khomidov, K.S. (1991). Purification and properties of membrane bound trehalase from silkworm eggs. Biochemistry (Moscow)., 56: 958-965.
Elbein, A.D., Pan,Y.T., Pasttuszak,I. and Carroll, D.(2003). New insights on trehalose: a multifunctional molecule. Glycobiology Journal,Oxford university press, 13: 17R- 27R.
Fonagy, A. (2009). Insect timing (rhythms) from the point of view of neuroendocrine effector mechanism. Acta. Phytopathologica et. Entomologica Hungarica., 44: 61-73.
Froy, O., Gotter, A. L., Casselman, A. L. and Reppert, S. M. (2003). Illuminating the circadian clock in monarch butterfly migration. Science, 300: 1303-1305.
Giebultowicz, J.M. (2001). Peripheral clocks and their role in circadian timing: insights from insects. Phil. Trans. R. Soc. Lond. B., 356: 1791-1799.
Gilby, A. R., Wyatt, S. S. and Wyatt, G. R. (1967). Trehalases from the cockroach, Blaberus discoidalis: activation, solubilization and properties of the muscle enzymes and some properties of the intestinal enzyme. Acta Biochim. Polon., 14: 83-100.
Goldsworthy,G. J. and Gade, G. (1983). The Chemistry of Hypertrehalosemic Factors. In: Downer, R. G. H., and Laufer, H (ed.), Endocrinology of Insects, New York: Alan R. Liss. pp. 109–119
Goto, M., Li,Y.P, Kayaba, S., Outani, S. and Suzuki, K. (2001). Cold hardiness in summer and winter diapauses and postdiapause pupae of the cabbage armyworm, Mamestra brassicae L. under temperature acclimation. Journal of Insect Physiol., 47: 709-714.
Hall, J. D. (2003). Genetics and Molecular Biology of Rhythms in Drosophila and other insects. Academic Press: Amesterdam. pp. 286
Han, R.D., Gan, Y. L., Kong, X. H. and Ge, F. (2008). Physiological and endocrine differences between diapauses and non diapausing larvae of the pine caterpillar Dengrolimus tabulaeformis (Lepidoptera: Lasicampidae). Zoological Studies, 47: 96-102.
Hirayama, J. and Sassone-Corsi, P. (2009). Transcription control and the circadian clock. Encyclopedia of Neuroscience. pp 1071-1080.
Huang, J., Furusawa, T., Sadakane, K. and Sugimura, Y. (2006). Purification and properties of two soluble trehalases from embryonic larvae of the silkworm, Bombyx mori. Journal of Insect Biotechnology and Sericology, 75: 1-8.
Ito,T. (1972). An approach to nutritional control mechanisms in silkworm, Bombyx mori. Israel J. Entomology, 7: 1-6.
Iwai, S., Fukui, Y., Fujiwara,Y. and Takeda, M. (2006). Structure and expressions of two circadian clock genes, period and timeless in the commercial silkmoth, Bombyx mori. J. Insect Physiol., 52: 625-637.
Iwami, M. (2000). Bombyxin: an insect brain peptide that belongs to the insulin family. Zool,Sci., 17: 1035-1044.
Jungreis, A. M. (1980). Hemolymph as a dynamic tissue. In: Locke, M., and Smith, D. S (ed.), Insect Biology in the Future. New York: Academic Press.pp 273–294
Kanamori, Y., Saito, A., Hagiwara-komoda, Y., Tanaka, D., Mitsumasu, K., Kikuta, S., Watanabe, M., Cornette, R. Kikawada, T. and Okuda, T. (2010). The trehalose transporter gene sequence is conserved in insects and encodes proteins with different kinetic properties involved in trehalose import into peripheral tissues. Insect Biochem and Mol Biol., 40: 30-37.
Khani, A., Moharamipour, S. and 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.
Kostal, V. and Shimada, K. (2001). Malfunction of circadian clock in the non- photoperiodic- diapauses mutants of the Drosophilid fly,Chymomyza costata. J. Insect Physiol., 47: 1269-1274.
Krishnaswami, S. (1986). New technology of silkworm rearing. Central Sericulture and Training Institute, Mysore, India.
Leevers, S. J. (2001). Growth control: invertebrate insulin surprises. Curr. Biol., 11: R 209- R 212.
Lokesh, G., Ananthanarayana, S.R. and Yoganandha murthy,V.N. (2012). Changes in the activity of digestive enzymes in respose to chemical mutagen diethyl sulfate in the silkworm Bombyx mori. L. (Lepedoptera: Bombycidae). Asian J. Applied Sci., 1-7.
Nagasawa, H., Kataoka, H. and Suzuki, A. (1990). Chemistry of Bombyx prothoracicotropic hormone and bombyxin. In: Ohnishi, E., and Ishizake, H (ed.), Molting and metamorphosis (pp 33-48), Berlin: Springler-Verlag.
Naidoo, N., Song, S., Hunter-ensor, M. and Sehgal, A. (1999). A role for the proteosome in the light response of the timeless clock protein. Science, 285: 1737-1741.
Narayanaswamy, T. K. and Shankar, M. A. (2010). Impact of organic based nutrient management on the activity of trehalase and protease enzymes in the midgut extract of silkworm, Bombyx mori. L. Mysore. J. Agric. Sci., 44: 272-275.
Nath, B.S. (2000) Changes in carbohydrate metabolism in haemolymph and fatbody of the silkworm, Bombyx mori L., exposed to organophorous insecticides. Pestic. Biochem.Physiol., 68:127-137.
Nijhout, H.F. (1994). Insect hormones. Princeton: Princeton university press.
Oda, Y., Uejuma, M., Iwami, M. and Sakurai, S. (2000). Involvement iof adipokinetic hormone in the homeostatic control of haemolllymph trehalose concentration in larvae of Bombyx mori. Arch. Insect Biochem. Physiol., 45: 156-165.
Orchard, I., Ramirez, J.M. and Lange, A.B. (1993). A multi functional role for octopamine in locust flight. Ann. Rev. Entomol., 38: 227-249.
Peschel, N., Chen, K. F., Szabo, G. and Sanewsky, R. (2009). Light dependent interactions between the Drosophila circadian clock factors cryptochrome, jetlag and timeless. Curr. Biol., 19: 241-247.
Roe, R. (1955). The determination of sugar in blood and spinal fluid with anthrone reagent. Journal of Biological Chemistry, 20: 335-343.
Roeder, T. (1999). Octopamine in invertebrates. Prog. Neurobiol., 59: 533-561.
Rulifson, E.J., Kim, S.K. and Nusse, R. (2002). Ablation of insulin producing neurons in flies: growth and diabetic phenotypes. Science, 296: 1118-1120.
Sailaja, B. and Sivaprasad, S. (2010) a. Photoperiodic modulation of circadian rhythms in the silk gland protein profiles of Bombyx mori and its influence on the silk productivity and quality. J. Appl & Nat. Science, 2: 48-56.
Sailaja, B. and Sivaprasad, S. (2010) b. Photoperiodic modulation of circadian protein rhythm in the silk gland of Bombyx mori during fourth instar development. The Bioscan, 5: 177-183.
Sailaja, B. and Sivaprasad, S. (2011). Photoperiod-induced clock shifting in the circadian protein and amino acid rhythm in the larval fat body of silkworm, Bombyx mori. J. Appl & Nat. Science, 3: 38-50.
Sailaja, B., Bhuvaneswari, E., Kavitha, S. and Sivaprasad, S. (2011). Photoperiod-induced clock shifting in the circadian protein and amino acid rhythm in the larval haemolymph of the silkworm, Bombyx mori. The Bioscan, 6: 355-363.
Saito, S. (1960). Trehalase of the silkworm, Bombyx mori: Purification and properties of the enzyme. J. Biochem., 48:101-109.
Satake, S., Masumura, M., Ishizaki, H., Nagata, K., Kataoka, H., Suzuki, A. and Mizoguchi, A. (1997). Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori. Comp. Biochem. Physiol., 118B: 349–357.
Satake, S., Nagata, K., Kataoka, H. and Mizoguchi, A. (1999). Bombyxin secretion in the adult silkmoth Bombyx mori: sex-specificity and its correlation with metabolism. J. Insect Physiol., 45: 939–945.
Saunders, D.S. (2002). Insect clocks, third edition (pp.560), Elsevier Science B.V.: Amsterdam.
Sehadova, H., Markova, E. P., Sehnal, F. and Takeda, M. (2004). Distribution of circadian clock related proteins in the cephalic nervous system of the silkworm, Bombyx mori. J. Biol. Rhythms, 19: 466-482.
Sharma,V. K. (2003). Adaptive significance of circadian clocks. Chronobiol. Int., 20: 901-919.
Shimizu, I. Kawai, Y., Tainguchi, M. and Aoki, S. (2001). Circadian Rhythm and cloning of the clock gene period in the honey bee Apiscerana japonica. Zoo. Sci., 18: 778-789.
Shiva kumar, G. and Shamitha, G. (2011). Comparative studies of trehalase activity in the outdoor and total indoor reared tasar silkworm, Antheraea mylitta drury (Daba TV). Asian. J. Exp. Biol. Sci., 2: 265-269.
Sivaprasad, S. and Sailaja, B. (2011). Photoperiod-modulated instar-specific clock-shifting in the circadian protein and amino acid rhythms in the larval segmental muscle of Bombyx mori. J. Appl. & Nat. Science, 3: 176-188.
Su, Z.H., Ikeda, M., Sato, Y. and Yamashita, O. (1993). Purification, C DNA cloning and nothern blot analysis of trehalase of pupal midgut of the silkworm, Bombyx mori. Biochem. Biophys. Acta., 1173: 217-224.
Sumida, M. and Yamashita, O. (1977). Trehalase transformation in silkworm midgut during metamorphosis. J. Comp. Physiol. B., 115: 241-253.
Sutherland, E.W. (1972). Studies on the mechanism of hormone action. Science, 177: 401-408.
Syrova, Z., Dolezel, D., Sauman, I., Hodokova, M. (2003). Photoperiodic regulation of diapauses in liden bugs: are period and clock genes are involved. Cell.Mol.Lif. Sci., 60: 2510-2515.
Tang, B., Chen, X., Liu, Y., Tian, H., Liu, J., Hu, J., Xu, W. and Zhang, W. (2008). Charecterization and expression patterns of a membrane-bound trehalase from Spoptera exigua. BMC Molecular Biology., 9: 51.
Terra,W R. and Ferreira,C . (2005). Biochemistry of digestion. Comprehensive Molecular Insect Science, Elsevier, 4: 171-224.
Thompson, S.N. (2003). Trehalose- The insect blood sugar. Advances in Insect Physiology, 31: 206-261.
Wyatt, G.R. (1967). The biochemistry of sugars and polysaccharides in insects. Adv. Insect Physiol., 4: 287-360.
Yamaoka, K., Hoshino, M. and Hirai, T. (1971). Role of sensory hairs on the anal papillae in oviposition behaviour of Bombyx mori. J. Insect Physiol., 47: 2327-2336.
Yamashita, O. (1965). Carbohydrate metabolism during embryonic development of the silkworm, Bombyx mori.L. The Journal of Sericultural Science of Japan, 34:1-8.
Yamashita, O. and Hasegawa, K. (1974). Mobilization of carbohydrates in tissues of female silkworms, Bombyx mori, during metamorphosis. J. Insect physiol., 20: 1749-1760.
Yanagawa, H. (1979). Effect of dietary levels of glucose on the metabolism of trehalose in the silkworm, Bombyx mori. The Journal of Sericultural Science of Japan, 48:461-468.
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