Abstract
Eggs of the plaice Pleuronectes platessa L. were incubated at temperatures of 5, 8, 10, 12 and 15°C in March 1990, 1991 and 1992. The myotomes of yolk-sac larvae contain a single superficial layer of small-diameter muscle fibres which stain intensely for succinic dehydrogenase activity, surrounding 390 to 500 weakly staining inner-muscle fibres of larger diameter. Larvae reared at 15°C only survived for a few days and had significantly more inner-muscle fibres of larger average cross-sectional area than those hatching at 5 to 10°C. Myofibrils occupied 61% of the volume of inner-muscle fibres in 15°C larvae compared with 35 and 36% in larvae hatching at 5 and 10°C, respectively (P(0.01). Following metamorphosis, which occurs between 7 and 10 wk, the myotomes retain the single layer of superficial-muscle fibres characteristic of larvae. A thickening of the superficial-muscle layer is first evident in 4 to 5 mo-old laboratory-reared fish of 20 mm total length (TL) and in 0-group fish caught in June and July. On the basis of the histochemical staining reactions for myofibrillar ATPase and succinic dehydrogenase activities, the myotomes of 1-group (104 mm TL) and adult (280 mm TL) plaice were found to contain a minimum of six distinct muscle-fibre types. Two-dimensional gel electrophoresis and peptide mapping were used to investigate changes in myosin subunit composition during development. Myosin from the inner muscle of larvae contains two isoforms of the phosphorylatable light-chain 2 (LC2L1 and LC2L2). Following metamorphosis and during the first year, inner-muscle fibres co-express LC2 isoforms characteristic of the superficial fast-muscle fibres of adult plaice (LC2F1 and LC2F2) in addition to the larval isoforms. Fast-muscle fibres isolated from deep layers of the myotomes in adult plaice only contain LC2F2. In contrast, myosin from larval muscle and adult fast muscle contain apparently identical alkali light chains (LC1 and LC3). Peptide maps of myosin heavy chains (MHCs) from 6 wk-old larvae and 10 wk-old fish that had completed metamorphosis are similar, but distinct from those of 1-group plaice. Further changes in white-muscle MHC composition are evident between 1-group fish of 104 mm TL and adults of 280 mm TL.
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References
Arnold, G. P., Weihs, D. (1978). The hydroynamics of rheotaxis in the plaice (Pleuronectes platessa L.). J. exp. Biol. 75: 147–169
Batty, R. S. (1984). Development of swimming movements and musculature of larval herring (Clupea harengus). J. exp. Biol. 110: 217–229
Beacham, T. D., Murray, C. B. (1987). Adaptive variation in body size, age, morphology, egg size and developmental biology of chum salmon (Oncorhynchus keta) in British Columbia. Can. J. Fish. aquat. Sciences 44: 244–261
Blaxter, J. H. S. (1986). Development of sense organs and behaviour of teleost larvae with special reference to feeding and predator avoidance. Trans. Am. Fish. Soc. 115: 98–114
Blaxter, J. H. S., Hempel, G. (1963). The influence of egg size on herring larvae (Clupea harengus L.). J. Cons. perm. int. Explor. Mer. 28: 211–240
Bloom, H., Beier, H., Gross, H. S. (1987). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93–99
Bone, Q., Johnston, I. A., Pulsford, A., Ryan, K. P. (1986). Contractile properties and ultrastructure of three types of muscle fibre in the dogfish myotome. J. Muscle Res. Cell Motil. 7: 47–56
Calvo, J., Johnston, I. A. (1992). Influence of rearing temperature on the distribution of muscle fibre types in the turbot Scophthalmus maximus at metamorphosis. J. exp. mar. Biol. Ecol. 161: 45–55
Crockford, T., Johnston, I. A. (1993). Developmental changes in the composition of myofibrillar proteins in the swimming muscles of Atlantic herring, Clupea harengus. Mar. Biol. 115: 15–22
Crockford, T., Wommack, K. E., Johnston, I. A., McAndrew, B. J., Mutungi, G., Johnson, T. P. (1991). Inter-and intra-specific variation in myosin light chain and troponin I composition in fast muscle fibres from two species of fish (genus Oreochromis) which have different temperature-dependent contractile properties. J. Muscle Res. Cell Motil. 12: 439–446
De Silva, C. (1974). Development of the respiratory system in herring and plaice larvae. In: Blaxter, J. H. S. (ed.) The early life history of fish. Springer Verlag, Berlin, New York, p. 465–485
El-Fiky, N., Hinterleitner, S., Wieser, W. (1987). Differentiation of swimming muscles and gills, and development of anaerobic power in the larvae of cyprinid fish (Pisces, Teleostei). Zoomorphology 107: 126–132
El-Fiky, N., Wieser, W. (1988). Lifestyles and patterns of development of gills and muscles in larval cyprinids (Cyprinidae; Teleostei). J. Fish Biol. 33: 135–145
Focant, B., Huriaux, F., Johnston, I. A. (1976). Subunit composition of fish myofibrils: the light chains of myosin. Int. J. Biochem. 7: 129–133
Focant, B., Huriaux, F, Vandewalle, P., Castelli, M., Goessens, G. (1992). Myosin, parvalbumin and myofibril expression in barbel (Barbus barbus L.) lateral white muscle during development. Fish Physiol. Biochem. 10: 133–143
Hovenkamp, F., Witte, J. I. J. (1991). Growth, otolith growth and RNA/DNA ratios of larval plaice, Pleuronectes platessa, in the North Sea 1987 to 1989. Mar. Ecol. Prog. Ser. 70: 105–116
Johnston, I. A. (1981). Quantitative analysis of muscle breakdown during starvation in the marine flatfish Pleuronectes platessa. Cell Tissue Res 214: 369–386
Johnston, I. A. (1993). Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae Mar. Biol. 116: 363–379
Johnston, I. A., Altringham, J. D. (1991). Movement in water: constraints and adaptations. In: Hochachka, P. W., Mommsen, T. P. (eds.) Biochemistry and molecular biology of fishes. Vol. 1. Elsevier Science Publishers, Amsterdam, New York, p. 249–268
Johnston, I. A., Horne, Z. (1993). Temperature and muscle development in the embryos and larvae of Atlantic herring (Clupea harengus; Teleostei). J. mar. biol. Ass. U.K. (in press)
Johnston, I. A., Patterson, S., Ward, P., Goldspink, G. (1974). The histochemical demonstration of myofibrillar adenosine triphosphatase activity in fish muscle. Can. J. Zool. 52: 871–877
Kilarski, W., Kozlowska, M. (1983). Ultrastructural characteristic of the teleostean muscle fibres and their nerve endings. The stickleback (Gasterosteus acleatus L.). Z. mikrosk.-anat. Forsch., Leipzig 97: 1022–1036
Lännergren, J. (1987). Contractile properties and myosin isozymes of various kinds of Xenopus twitch muscle fibres. J. Muscle Res. Cell Motil. 8: 260–273
Mahoney, R. (1966). Laboratory techniques in zoology. Butterworths, London
Matsuoka, M., Iwai, T. (1984). Development of the myotomal musculature in the red sea bream. Bull. Jap. Soc. scient. Fish. 50: 29–35
Nachlas, M. M., Tsou, K. C., De Sonsa, E., Cheng, C. S., Seligman, A. M. (1957). Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J. Histochem. Cytochem. 5: 420–436
Neuhoff, J., Arold, N., Taube, D., Ehrhardt, W. (1988). Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255–262
O'Connell, C. P. (1981). Development of organ system in the northern anchovy, Engraulis mordax, and other teleosts. Am. Zool. 21: 429–446
Osse, J. W. M. (1990). Form changes in fish larvae in relation to changing demands of function. Neth. J. Zool. 40: 429–385
Pearse, A. G. E. (1960). Histochemistry, 2nd edn. Churchill Livingstone, Edinburgh
Reiser, P. J., Greaser, M. L., Moss, R. L. (1988). Myosin heavy chain composition of single cells from avian slow skeletal muscle is strongly correlated with velocity of shortening during development. Devl. Biol. 129: 400–407
Ryland, J. S., Nichols, J. H. (1967). Effect of temperature on the efficiency of growth of plaice prolarvae. Nature, Lond. 214: 529–530
Ryland, J. S., Nichols, J. H., Sykes, A. M. (1975). Effect of temperature on the embryonic development of the plaice, Pleuronectes platessa L. (Teleostei). J. exp. mar. Biol. Ecol. 18: 121–137
Scapolo, P. A., Veggetti, A., Mascarello, F., Romanello, M. G. (1988). Developmental transitions of myosin isoforms and organisation of the lateral muscle in the teleost Dicentrarchus labrax (L.). Anat. Embryol. 178: 287–296
Stickland, N. C., White, R. N., Mescall, P. E., Crook, A. R., Thorpe, J. E. (1988). The effect of temperature on myogenesis in embryonic development of the Atlantic salmon (Salmo salar L.). Anat. Embryol. 178: 253–257
Van Raamsdonk, W., Pool, C. W., te Kronnie, G. (1978). Differentiation of muscle fibre types in the teleost Brachydanio rerio. Anat. Embryol. 153: 137–155
Veggetti, A., Mascarello, F., Scapolo, P. A., Rowlerson, A. (1990). Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax. An ultrastructural and morphometric study. Anat. Embryol. 182: 1–10
Vieira, V. L. A., Johnston, I. A. (1992). Influence of temperature on muscle-fibre development in larvae of the herring Clupea harengus. Mar. Biol. 112: 333–341
Waterman, R. E. (1969). Development of the lateral musculature in the teleost Brachydanio rerio: a fine structural study. Am. J. Anat. 125: 457–494
Weibel, E. R. (1989). Stereological methods. Vol. 1. Practical methods for biological morphometry. Academic Press, London
Williams, P. J., Brown, J. A. (1992). Development changes in the escape response of larval winter flounder Pleuronectes americanus from hatch through metamorphosis. Mar. Ecol. Prog. Ser. 88: 185–193
Yancey, P. H., Johnston, I. A. (1982). Effect of electrical stimulation and exercise on the phosphorylation state of myosin light chains from fish skeletal muscle. Pflügers Arch. 393: 334–339
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Brooks, S., Johnston, I.A. Influence of development and rearing temperature on the distribution, ultrastructure and myosin sub-unit composition of myotomal muscle-fibre types in the plaice Pleuronectes platessa . Marine Biology 117, 501–513 (1993). https://doi.org/10.1007/BF00349326
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DOI: https://doi.org/10.1007/BF00349326