Photoperiod-modulated instar-specific clock-shifting in the circadian protein and amino acid rhythms in the larval segmental muscle of Bombyx mori
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Abstract
The photoperiod-modulated clock-shifting in the circadian protein rhythm was studied in the segmental muscle of Bombyx mori. The analysis of phase response curves of the fourth instar rhythm revealed that the muscle tissue completes six protein synthetic cycles (PS cycles) under normal 12 hr light and 12 hr dark cycle (LD), 8 cycles each under continuous light (LL) and continuous dark (DD) conditions. The fifth instar protein rhythm showed seven PS cycles each under LD and DD conditions, but only six under LL. The protein rhythm gets clock-shifted in instarspecific and photoperiod-specific fashions. In the fourth instar, both LL and DD conditions advanced the 24 hr free running time of the rhythm by six hours and set it at 18 hr, but in the fifth instar it is delayed by 4 hr and set at ~28 hr under LL, but remained unchanged under DD. Comparative analysis of protein and amino acid profiles shows that the photoperiod modulates the protein rhythm by altering the rate of amino acid mobilization.
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Keywords
Bombyx mori, Circadian amino acid rhythm, Circadian protein rhythm, Segmental muscle, Photoperiod
References
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Gizelak, K. (1995). Control of expression of silk protein genes. Comp. Biochem. Physiol. B: Biochem. Mol. Boil., 110: 671-681.
Grima, B., Chelot, B.E., Xia, R. and Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature, 431: 862-868.
Hall, J.D. (2003). Genetics and Molecular Biology of Rhythms in Drosophila and other insects. Academic Press, Amsterdam, pp 286.
Hou, Y., Zou, Y., Wang, F., Gong, J., Zhong, X., Xia, Q. and Zhao, P. (2010). Comparative analysis of proteome maps of silkworm haemolymph during different developmental stages. Proteome Sci., 8: 45.
Ishikawa, E. and Suzuki,Y. (1985). Tissue and stage-specific expression of sericin genes in the middle silk gland of Bombyx mori. Dev. Growth Diff., 27: 73-82.
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(6): 625-637.
Kawasaki, F. and Kita, H. (2004). Structure and innervation of longitudinal and transverse abdominal muscles of the cricket, Gryllus bimaculatus. J.Comp.Neurol., 352(1): 134-146.
Kimura, K., Oyama, F., Ueda, H., Mizuno ,S. and Shimura, K. (1985). Molecular cloning of the fibroin light chain complementary DNA and its use in the study of the expression of the light chain gene in the posterior silk gland of Bombyx mori. Experientia, 41: 1167-1171.
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Lowry, O.H., Rosenbrough, N.J., Farra, L. and Randall, R.J. (1951). Protein measurement with Folin phenol reagent. J. Biol. Chem., 1933: 265-275.
Michaille, J.J., Garel, A. and Prudhomme, J.C. (1989). The expression of five middle silk gland specific genes is territorially regulated during the larval development of Bombyx mori. Insect Biochem., 19: 19-27.
Moore, S. and Stein, W.A. (1954). A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem., 211: 907-913.
Obara, T. and Suzuki, Y. (1988). Temporal and spatial control of silk gene transcription analyzed by nuclear run-on assay. Devl. Biol., 127: 384-391.
Peschel, N., Chen, K.F., Szabo, G. and Stanewsky, R. (2009). Light-dependent interactions between the Drosophila circadian clock factors cryptochrome, jetlag and timeless. Curr. Biol., 19 (3): 241- 247.
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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. Sci., 2 (1): 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 (2): 177 – 183.
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.
Shafer, T.O., Levine, J.D., Truman, J.W. and Hall, J.C. (2004). Flies by night: Effects of changing day length on Drosophila’s circadian clock. Curr. Biol.,14 (5): 424–432.
Sivaprasad, S. (2010). Origin and peripheral distribution of the thoracic and abdominal median nerves in the fifth instar larva of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). J. Appl. & Nat. Sci., 2 (2): 251-257
Sivaprasad, S. and Muralimohan, P. (2009 a). Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori(Lepidoptera: Bombycidae): I. Cephalothoracic musculature and its innervation. J. Appl. & Nat. Sci., 1(2): 201-209.
Sivaprasad, S. and Muralimohan, P. (2009 b). Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori (Lepidoptera: Bombycidae): II. Abdominal musculature and its innervation. J. Appl. & Nat. Sci., 1 (2): 210-226.
Stoleru, D., Peng, Y., Agosto, J. and Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature, 431: 862-868.
Syrova, Z., Dolezel, D., Saumann, I. and Hodkova, M. (2003). Photoperiodic regulation of diapause in linden bugs: Are period and Clock genes involved? Cell. Mol. Life Sci., 60: 2510-2515.
Triplehorn, C.A. and Johnson, N.F. (2005). Borror and DeLong’s Introduction to the Study of Insects (7th Edition), Brooks / Thomson Cole, USA.
Xu, K., Zheng, X. and Seghal, A. (2008). Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metabolism, 8 : 289-300.
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.
Zhang, P. B., Aso, Y.K., Jikuya, H., Kusakabe, T., Lee, J.M., Kawaguchi, Y., Yamamoto, K., Banno, Y. and Fujii, H. (2007). Proteomic profiling of the silkworm skeletal muscle proteins during larval-pupal metamorphosis. J. Proteome Res., 6 (6): 2295-303.
Fukuta, M., Matsuno, K., Hui, C., Nagata, T., Takiya, S., Xu, P. X., Ueno, K. and Suzuki,Y. (1993). Molecular cloning of a POU domain-containing factor involved in the regulation of the Bombyx sericin-1 gene. J. Boil. Chem., 268: 19471-19475.
Gizelak, K. (1995). Control of expression of silk protein genes. Comp. Biochem. Physiol. B: Biochem. Mol. Boil., 110: 671-681.
Grima, B., Chelot, B.E., Xia, R. and Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature, 431: 862-868.
Hall, J.D. (2003). Genetics and Molecular Biology of Rhythms in Drosophila and other insects. Academic Press, Amsterdam, pp 286.
Hou, Y., Zou, Y., Wang, F., Gong, J., Zhong, X., Xia, Q. and Zhao, P. (2010). Comparative analysis of proteome maps of silkworm haemolymph during different developmental stages. Proteome Sci., 8: 45.
Ishikawa, E. and Suzuki,Y. (1985). Tissue and stage-specific expression of sericin genes in the middle silk gland of Bombyx mori. Dev. Growth Diff., 27: 73-82.
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(6): 625-637.
Kawasaki, F. and Kita, H. (2004). Structure and innervation of longitudinal and transverse abdominal muscles of the cricket, Gryllus bimaculatus. J.Comp.Neurol., 352(1): 134-146.
Kimura, K., Oyama, F., Ueda, H., Mizuno ,S. and Shimura, K. (1985). Molecular cloning of the fibroin light chain complementary DNA and its use in the study of the expression of the light chain gene in the posterior silk gland of Bombyx mori. Experientia, 41: 1167-1171.
Krishnaswami, S. (1986). New technology of silkworm rearing. Central Sericultural Research and Training Institute, Mysore, India.
Lowry, O.H., Rosenbrough, N.J., Farra, L. and Randall, R.J. (1951). Protein measurement with Folin phenol reagent. J. Biol. Chem., 1933: 265-275.
Michaille, J.J., Garel, A. and Prudhomme, J.C. (1989). The expression of five middle silk gland specific genes is territorially regulated during the larval development of Bombyx mori. Insect Biochem., 19: 19-27.
Moore, S. and Stein, W.A. (1954). A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem., 211: 907-913.
Obara, T. and Suzuki, Y. (1988). Temporal and spatial control of silk gene transcription analyzed by nuclear run-on assay. Devl. Biol., 127: 384-391.
Peschel, N., Chen, K.F., Szabo, G. and Stanewsky, R. (2009). Light-dependent interactions between the Drosophila circadian clock factors cryptochrome, jetlag and timeless. Curr. Biol., 19 (3): 241- 247.
Sailaja, B. and Sivaprasad, S. (2011). Photoperiod-induced clock-shifting in the circadian protein and amino acid rhythms in the larval fat body of silkworm, Bombyx mori. J. Appl. & Nat. Sci., 3 (1): 38-50.
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. Sci., 2 (1): 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 (2): 177 – 183.
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.
Shafer, T.O., Levine, J.D., Truman, J.W. and Hall, J.C. (2004). Flies by night: Effects of changing day length on Drosophila’s circadian clock. Curr. Biol.,14 (5): 424–432.
Sivaprasad, S. (2010). Origin and peripheral distribution of the thoracic and abdominal median nerves in the fifth instar larva of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). J. Appl. & Nat. Sci., 2 (2): 251-257
Sivaprasad, S. and Muralimohan, P. (2009 a). Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori(Lepidoptera: Bombycidae): I. Cephalothoracic musculature and its innervation. J. Appl. & Nat. Sci., 1(2): 201-209.
Sivaprasad, S. and Muralimohan, P. (2009 b). Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori (Lepidoptera: Bombycidae): II. Abdominal musculature and its innervation. J. Appl. & Nat. Sci., 1 (2): 210-226.
Stoleru, D., Peng, Y., Agosto, J. and Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature, 431: 862-868.
Syrova, Z., Dolezel, D., Saumann, I. and Hodkova, M. (2003). Photoperiodic regulation of diapause in linden bugs: Are period and Clock genes involved? Cell. Mol. Life Sci., 60: 2510-2515.
Triplehorn, C.A. and Johnson, N.F. (2005). Borror and DeLong’s Introduction to the Study of Insects (7th Edition), Brooks / Thomson Cole, USA.
Xu, K., Zheng, X. and Seghal, A. (2008). Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metabolism, 8 : 289-300.
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.
Zhang, P. B., Aso, Y.K., Jikuya, H., Kusakabe, T., Lee, J.M., Kawaguchi, Y., Yamamoto, K., Banno, Y. and Fujii, H. (2007). Proteomic profiling of the silkworm skeletal muscle proteins during larval-pupal metamorphosis. J. Proteome Res., 6 (6): 2295-303.
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Photoperiod-modulated instar-specific clock-shifting in the circadian protein and amino acid rhythms in the larval segmental muscle of Bombyx mori. (2011). Journal of Applied and Natural Science, 3(2), 176-188. https://doi.org/10.31018/jans.v3i2.177
