FUNCTIONAL DEVELOPMENT OF THE RETICULAR SYSTEM IN AN INSECT MUSCLE WITH SYNCHRONOUSLY DIFFERENTIATING CELLS
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1 J. Cell Sci. 12, (i973) 197 Printed in Great Britain FUNCTIONAL DEVELOPMENT OF THE RETICULAR SYSTEM IN AN INSECT MUSCLE WITH SYNCHRONOUSLY DIFFERENTIATING CELLS N. M. TYRER Department of Neurobiology, Research School of Biological Sciences, Australian National University, Box 475, Canberra, Australia SUMMARY In contrast to many developing muscles which contain a spectrum of cells at different stages of differentiation, cell development in the locust abdominal intersegmental muscle tends to be synchronous, so that at any stage of development the cells are at the same stage of differentiation. This makes it feasible to relate the properties of the developing tissue as a whole to changes occurring within the cells. Muscle contraction in the abdominal dorsal muscles of locust embryos and young hoppers has been related to ultrastructural changes within the muscle. Early in development both contraction and relaxation rates are very slow and the muscle shortens very little. The maximum registered tension is achieved relatively early while the rates of contraction and relaxation remain slow. Contraction and relaxation become more rapid as the embryo develops. These changes can be related to the development of the reticular system, various components of which mature at different rates. When the muscle is first able to develop tension the myofibres contain scattered clusters of myofilaments while the transverse tubule system (T-system), the cisternae and the sarcoplasmic reticulum (SR) are not well developed. The myofibres reach their final size and the filaments are fully formed while the T-system is still irregular and the SR is sparse. The T-system and the cisternae become well developed before the SR. During the time that the relaxation time decreases the SR becomes increasingly prominent. INTRODUCTION Physiological and biochemical features of developing muscle have been studied extensively in vertebrates (e.g. Buller, Eccles & Eccles, i960; Close, 1964; Trayer & Perry, 1966; Klicka & Kasper, 1970; Dow & Stracher, 1971; Margreth, Salviati & Catani, 1971). Ultrastructural changes in developing vertebrate muscle have also been described (Allen & Pepe, 1965; Ezerman & Ishikawa, 1967; Shimada, Fischman & Moscona, 1967; Fischman, 1967; Shiaffino & Margreth, 1969; Edge, 1970) and in some cases it has been possible to correlate these changes with the changing properties of the muscle (Aloisi & Margreth, 1967; Luff & Atwood, 1971). In vertebrates 2 problems are encountered when making detailed comparison between the changing ultrastructure and the changing properties of developing muscle. First, many adult muscles contain a heterogeneous population of muscle fibre types, usually described as red, white and intermediate (Edgerton & Simpson, 1969). The different developmental histories of these fibre types may confuse attempts to relate
2 198 N. M. Tyrer cellular changes with the changing properties of the whole muscle. Secondly, many developing muscles contain a spectrum of cells at different stages of differentiation (Allen & Pepe, 1965; Kelly, 1971) which precludes direct correlation between cell development and the physiological or biochemical features of the muscle as a whole. In this paper an insect muscle is described in which the differentiation, of the cells is synchronous. All cells at any particular stage of development are at the same stage of differentiation. This offers a unique possibility for the study of development of physiologically important components of muscle cells. The development of the time course of contraction and relaxation of this muscle has been investigated, which is the subject of a preliminary report (Tyrer, 1969). It is found that development of tension, contraction rate and relaxation rate all occur separately at easily identifiable stages, which can be related to developments in the structure of the muscle. MATERIALS AND METHODS Eggs and hoppers were obtained from a culture of the locust Schistocerca gregaria maintained in the Department of Zoology, Cambridge, England, under conditions similar to those used by the Anti-Locust Research Centre (now Centre for Overseas Pest Research) (Hunter-Jones, 1961). Definition and identification of developmental stages The eggs of S. gregaria are laid in pods of 30 to 90. The development time of different pods of embryos is variable, so that the age of an embryo is not a precise way of describing the stage of development. Fortunately, all the eggs in any one pod tend to develop at the same rate (Tyrer, 1970) so it is possible to define the stage of development of an embryo as a percentage of the incubation period of the egg pod from which it came. Using this method, a newly hatched hopper is described at 100 %, while an embryo which is three-quarters developed is a 75 % embryo. Two methods, which are described elsewhere, were used to stage embryos (Tyrer, 1970). Either the stage was calculated from accurate measurements of the times when the egg pod was laid and when the first hopper hatched (= timed), or the percentage development was estimated from external morphological criteria (= estimated). Measurement of the mechanical response of the muscles The dorsal longitudinal intersegmental muscles from the fourth abdominal segment were used (Fig. 1). Details of the methods used to record the mechanical response of these muscles in the embryo are described elsewhere (Tyrer, 1969). The dorsal part of one side of the fourth abdominal segment was isolated mechanically from the rest of the abdomen and hooked to the recording lever system. The response of the muscles to stimulation of their motor nerve with a burst of stimuli for 0-7 s at a frequency of 50/s was recorded (Fig. 2). Responses of the muscles were recorded from 40 preparations. Sixteen of these were made from animals whose age was calculated as a percentage of the total development time. These preparations were from the period of development %. Twenty-four preparations were from animals whose age was estimated on morphological criteria. Four of these were at the 70% stage, 6 at 80, 7 at 93 and 7 at the 100 % stage. The relaxation time from peak tension to half the peak tension, T R, was measured during 12 maximal responses for each preparation. It is not possible to compare quantitatively the contraction times and degree of tension developed at different stages of development since the stimulus used may have imposed false minima on these values in the later stages of development.
3 Development of locust SR % 80% 92% Dorsal muscles 100% 1 mm 109% 40 A 1 s Fig. 1 Fig. 2 Fig. 1. Diagram of a newly hatched hopper dissected to show the position of the dorsal intersegmental muscles. Those in the fourth segment are shown in black. The development of the dorsal muscles of other segments parallels that of the fourth. Fig. 2. Examples of the response of the dorsal muscles to stimulation of their motor nerve at a frequency of 50/s for 0-7 s at different stages of development. (Base lines and stimulus artifacts are retouched.) Electron microscopy The dorsal muscles from the fourth abdominal segment (Fig. 1) of several embryonic stages, of the 100 % stage and the 5-day-old first instar hopper, were prepared for electron microscopy. In an initial investigation material was obtained from accurately timed embryos and was calculated to be from the 68, 77 and 92 % stages of development. Subsequently, material was obtained from embryos which were staged according to morphological criteria. Stages estimated to be 70, 80 and 92 % were used (Tyrer, 1970). The 5-day-hopper material was from animals in which the development time of the embryos was unknown. Embryos and hoppers were decapitated and a mid-dorsal incision made along the length of the body. The body wall was pinned out, well extended, on plasticine in a dish and fixed for 2 h in ice-cold glutaraldehyde fixative. This comprised 2-5 % glutaraldehyde maintained at ph 7-0 in 0-05 M sodium cacodylate buffer containing 0-17 M sucrose. After overnight washing in cold sodium cacodylate-buffered 0-34 M sucrose, the material was treated with sodium cacodylate-buffered 1 % osmium tetroxide at ph 7-0 for 1 h, dehydrated in an ethanol series and embedded in Araldite. For examination with the light microscope i-/«n thick sections were cut with glass knives, dried down on to microscope slides, and stained either with 1 % methylene blue in 1 % borax or with 1 % toluidine blue in 1 % borax. For electron microscopy thin
4 200 N. M. Tyrer 40 r 30 \ % development Fig. 3. The time of relaxation from peak to half peak tension of the dorsal muscles at different stages of development. The mean of 12 responses is shown for each preparation. The responses were obtained by maximal stimulation of the motor nerve at a frequency of 50/s for 0-7 s (see Fig. 2). The stages defined according to morphological criteria are shown as open symbols and the timed stages as closed symbols. The limits indicated are 2 standard deviations from the mean. sections were cut using glass knives and either a Huxley or a Reichert ultramicrotome. Contrast was enhanced by double staining, initially with saturated uranyl acetate in 50 % ethanol (1-5 h) and subsequently with Reynold's lead citrate (0-5 h). Longitudinal sections proved to be particularly difficult to stain. Some success was achieved by pretreating the sections with amyl acetate vapour for 0-5 h and then staining for 3 h in uranyl acetate and 1 h in lead citrate. Even so, satisfactory contrast was obtained only in relatively thick sections. Sections were examined either with a Philips EM 200 or a Hitachi HU11E electron microscope. RESULTS The time course of the muscle response The youngest preparation from which a mechanical response was obtained on stimulation of the dorsal nerve was a 67% embryo. Shortening was slight and the contraction and relaxation times were long and variable (Figs. 2, 3). In older preparations, shortening increased, until by the 80% stage the muscle shortened to the same extent and developed the same tension as in the newly hatched animal (Fig. 2). In the 80% embryo, however, both contraction and relaxation times of the responses were still longer and more variable than those of the newly hatched animal (Figs. 2, 3). Not only was there variation from preparation to preparation, but different records from the same preparation gave variable results. In older stages contraction and relaxation times became progressively shorter and variation was considerably reduced. While the relaxation rate continued to increase throughout
5 Development of locust SR 201 the period of development investigated, there appeared to be little change in the contraction rate after the 92% stage (Fig. 2). The ultrastructure of the muscle There are 2 surprising features in the developing intersegmental muscle. First, the differentiation of the myofibres in any one muscle is synchronous. Virtually no differences could be detected in the organization of the individual myofibres in any given muscle. Secondly, except in the earliest embryos, the myofibre is the only cell type present in the muscle (excluding nerves and their sheath cells (Figs. 8, 12, 16, 20)). In each of the 4 dorsal muscles there are between 9 and 20 myofibres usually arranged in 2 rows (Figs. 4, 8, 12, 16, 20). In all stages later than 80% these are generally between 10 and 15 /tm in diameter and about 0-5 mm long. Earlier than the 80% stage the myofibres are smaller in cross-section - between 5 and 8/tm in diameter in the 70% stage (Fig. 4), but they are the same length as in later stages. In these early stages, myoblasts are present although all the myofibres are at the same stage of differentiation. The number of myoblasts decreases as the myofibres increase in size until by the 80% stage they are very rare. Presumably the fusion of the myoblasts with the myofibres results in the increase in their diameter as occurs in other insect muscles during development (Crossley, 1972). The organization of the myofibre In mature locust intersegmental muscle, as in many insect skeletal muscles (see Mill & Lowe, 1971), the sarcomere is long, 7-8 /tm, the Z-bands are irregular and imprecisely aligned in adjacent fibrils, and there are 9-12 thin filaments surrounding each thick filament. The myofilaments occur in groups, myofibrils, which are between 0-5 and i-o/tm in diameter. Surrounding each myofibril in the A-band region is a network of tubules, the sarcoplasmic reticulum (SR), communicating with cisternae which occur close to the junction between the A-band and the I-band. In this region also the transverse tubules (T-tubules) descend from the external membrane and are closely apposed to the cisternae in such a way that, in section, 2 profiles are seen, one of the T-tubule and the other of the cisternal element. This is the dyad, which is analagous to the triad found in vertebrate reticular system. Mitochondria occupy the space between the myofibrils in the I-band region but they are sparsely distributed and so are not seen between every myofibril in any one section. The 70% stage (Figs. 4-7) Already by this stage the myofilaments are organized into sarcomeres of the same dimensions as in the mature muscle (Fig. 6). The myofilaments are grouped into myofibrils which may be up to 1 /tm in diameter, although they are usually rather smaller than this (Figs. 5, 7). The myofibrils are separated by large areas of sarcoplasm which contain a few membrane-bound profiles, some irregularly oriented filaments, ribosomes and an occasional microtubule (Figs. 6, 7). Mitochondria, as yet
6 202 N. M. Tyrer small and containing few cristae, are arranged irregularly on either side of the Z-band (Fig. 6). The reticular system at this stage is poorly developed. The outer cell membrane is invaginated in a few places to form T-system elements about 40 nm in diameter, but there are few of these and they usually extend only a short distance into the cells (Figs. 5, 7). Between the myofibrils a few thin-walled profiles, without contents, are seen in the A-band region, and these appear to be the beginning of the SR (Fig. 6). Irregularly shaped, thin-walled elements are associated with the T-system elements in the A-I band region. Sometimes these elements have weakly electron-dense contents and have electron-dense material between them and the T-tubule: this suggests that differentiation of cisternal elements has begun (Figs. 6, 7). Membrane structures similar to those associated with the T-tubules frequently approach the plasma membrane and run parallel to it (Fig. 7). These resemble the peripheral couplings described in developing rat intercostal muscle by Kelly (1971)- The 80% stage {Figs. 8-11) As can be seen in transverse sections, the sarcoplasm is now packed with myofilaments (Fig. 9). The myofibrils are, as in the previous stage, still usually o/tm across, but a greater proportion are closer to 1 jum across than in the 70% embryo. Some of the peripheral myofibrils may be a little larger. No change in the myofibril size occurs in subsequent stages. Between the myofibrils profiles of SR are sparse, but a small number of cisternae are easily identified associated with T-tubules in the A-I band region (Fig. 9). They form flattened sacs about 60 nm across, usually have weakly electron-dense contents and frequently have electron-dense material interposed between them and the T-tube. Peripheral couplings of SR elements and the surface are rare at this stage. Some of the tubes of the T-system descending from the plasma membrane extend much deeper into the cell than before while others are still ill-developed. Mitochondria are still fairly small and have few cristae. The 92% stage (Figs ) The reticular elements are now relatively well differentiated. The plasma membrane is invaginated at regular intervals around the fibre and the T-tubules descend uniformly into the fibre (Fig. 13). Dyads at the A-I band region are well formed and numerous and the contents of the cisternae are more electron-dense than in earlier stages (Fig. 13). The dyads now appear to be fully developed (Figs. 14, 15). No change in their structure or number occurs after this stage. In the A-band region, however, the SR is still sparse. Mitochondria are larger and contain more cristae (Fig- 13)- The 100% stage (Figs ) The most important difference between the 100 and 92% stage is the increased development of the SR. The profiles of the tubules between the myofibrils in the A-band region are better defined and rather more numerous (Fig. 17). The organiza-
7 Development of locust SR 203 tion of the T-system and dyads, however, is little changed. Mitochondria have more cristae than in earlier stages (Figs. 17, 18) and the variability of their shape in transverse section (Fig. 17) suggests that they now have a more complicated structure than the simple cylindrical condition in the earlier embryonic stages. They may bear processes like those described in cockroach femoral muscle (Hagopian, 1966). The 5-day stage (Figs ) A striking difference between this stage and the earlier ones is the abundance of the SR. Whereas the region between myofibrils previously contained SR which was one or two profiles wide, in this stage there are tiers of 4 and even 5 profiles. Other features of the muscle are little changed. DISCUSSION Structurally the myofilaments appear to have attained their full development by the 80% embryonic stage even though the T-system and SR are still poorly developed. By the 92 % stage the T-system and dyads are as highly organized as in later stages, while the SR is still sparse. In subsequent stages the SR continues to develop and by the 5-day stage has become quite elaborate. Concepts of the roles of the various components of the reticular system in insects (Smith, 1966) have been based largely on cytological similarities with vertebrates (see Peachey, 1968). Thus, it is assumed that in insects, as in vertebrates, the T-system conveys a signal into the cell following surface excitation, which, at the dyad, causes calcium to be released into the sarcoplasm. from the cisternae, so causing the myofilaments to contract. Relaxation is supposed to be achieved, as in vertebrates, by rapid uptake of calcium into the SR which then returns it to the cisternae. The experimental observations on the developmental changes in relaxation rate in this muscle correlate well with the structural changes in the SR. The mean values for the relaxation rate, T^R, (Fig. 3) decrease progressively at the same time that the SR elaborates. This supports the supposition that the process of relaxation in this insect is similar to that in vertebrates. There is also a progressive increase in the rate of contraction as development proceeds, particularly in the early stages. It appears, under these experimental conditions, that the maximal contraction rate is attained before the maximal relaxation rate (Fig. 2). It may be significant that the T-system and dyads appear to be fully formed before the SR is fully developed, although of course, SR development should also affect the contraction time since the rate at which the SR accumulates calcium is a factor determining when contraction ends. A possibility which must be considered is that the time course of the membrane potential produced by stimulating the motor nerve may be slower in the earlier stages of development. Microelectrode recordings from the muscle during stimulation of the nerve showed no change in the time course of the membrane response between the 92 and 100% stages (Tyrer, 1968, 1969). Records were not obtained, however, from earlier embryos so this remains a possible explanation for all or part of the slower time course of the mechanical response in the earlier stages.
8 204 N. M. Tyrer Other factors which have not been considered here may affect the time course of the mechanical response during development. Changes may occur in the contractile proteins themselves, or in the metabolism of the muscle. These questions can only be answered by further analysis of the properties of the muscle. Such detailed analyses of the biophysical, biochemical and physiological changes during development are feasible in these muscles because of the synchronized differentiation of the muscle cells. The initial investigation for this study was done as part of a Ph.D. dissertation in the Department of Zoology in the University of Cambridge, while I held a Research Studentship from the Agricultural Research Council. I am indebted to Dr J. E. Treherne for his advice and encouragement during this period and for allowing me the facilities of the A.R.C. unit in the Department of Zoology, Cambridge, in 1971 to obtain the material to finish the work in Australia. I am grateful to Miss A. B. Poyser and Mr R. Whitty for their skilled technical assistance. I thank my wife Dr J. Altman for continually pressing me to publish the work and for reading the manuscript. REFERENCES ALLEN, E. R. & PEPE, F. A. (1965). Ultrastructure of developing muscle cells in the chick embryo. Am. J. Anat. 116, ALOISI, M. & MARGRETH, A. (1967). In Exploratory Concepts in Muscular Dystrophy and Related Disorders (ed. A. T. Milhorat), pp Amsterdam: Exerpta Medica Foundation, International Congress Series 147, BULLER, A. J., ECCLES, J. C. & ECCLES, R. M. (i960). Differentiation of fast and slow muscles in the cat hind-limb. J. Physiol., Lond. 150, CLOSE, R. (1964). Dynamic properties of fast and slow skeletal muscles of the rat during development. J. Physiol., Lond. 173, CROSSLEY, A. C. (1972). Ultrastructural changes during transition of larval to adult intersegmental muscle at metamorphosis in the blow-fly, Calliphora erythrocephala. I. Dedifferentiation and myoblast fusion. J. Embryol. exp. Morph. 27, Dow, J. & STRACHER, A. (1971). Changes in the properties of myosin associated with muscle development. Biochemistry, N.Y. 10, EDGE, M. B. (1970). Development of apposed sarcoplasmic reticulum at the T system and sarcolemma and the change in orientation of triads in rat skeletal muscle. Devi Biol. 23, EDGERTON, V. R. & SIMPSON, D. R. (1969). The intermediate muscle fibre of rats and guinea pigs. J. Histochem. Cytochem. 17, EZERMAN, E. B. & ISHIKAWA, H. (1967). Differentiation of the sarcoplasmic reticulum and T-system in developing chick skeletal muscle in vitro. J. Cell Biol. 35, FISCHMAN, D. A. (1967). An electron microscope study of myofibril formation in embryonic chick skeletal muscle. J. Cell Biol. 32, HAGOPIAN, M. (1966). The myofilament arrangement in the femoral muscles of the cockroach Leucophaea maderae Fabricius. J. Cell Biol. 28, HUNTER-JONES, P. (1961). Rearing and Breeding Locusts in the Laboratory, pp London: Anti-Locust Research Centre. KELLY, A. M. (1971). Sarcoplasmic reticulum and T tubules in differentiating rat skeletal muscle. J. Cell Biol. 49, KLICKA, J. & KASPA, J. L. (1970). Changes in enzyme activities of the hatching muscle of the chick (Gallus domesticus) during development. Comp. Biochem. Physiol. 36, LUFF, A. R. & ATWOOD, H. L. (1971). Changes in the sarcoplasmic reticulum and transverse tubular system of fast and slow skeletal muscles of the mouse during postnatal development. J. Cell Biol. 51,
9 Development of locust SR 205 MARGRETH, A., SALVIATI, G. & CATANI, C. (1971). Electron transport in sarcoplasmic reticulum of fast and slow muscles. Archs Biochem. Biophys. 144, MILL, P. J. & LOWE, D. A. (1971). Ultrastructure of the respiratory and non-respiratory dorsoventral muscles of the larva of a dragonfly. J. Insect Physiol. 17, PEACHEY, L. D. (1968). Muscle. A. Rev. Physiol. 30, SHIAFFINO, S. & MARGRETH, A. (1969). Co-ordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J. Cell Biol. 41, SHIMADA, Y., FISCHMAN, D. A. & MOSCONA, A. A. (1967). The fine structure of embryonic chick skeletal muscle cells differentiated in vitro. J. Cell Biol. 35, SMITH, D. S. (1966). The organisation and function of the sarcoplasmic reticulum and T-system of muscle cells. Prog. Biophys. molec. Biol. 16, TRAYER, I. P. & PERRY, S. V. (1966). The myosin of developing skeletal muscle. Biochem. Z. 345, TYRER, N. M. (1968). Some Aspects of Functional Development in the Locust Embryo. Ph.D. Thesis University of Cambridge. TYRER, N. M. (1969). Time course of contraction and relaxation in embryonic locust muscle. Nature, Lond. 224, TYRER, N. M. (1970). Quantitative estimation of the stage of embryonic development in the locust, Schistocerca gregaria. J. Embryol. exp. Morph. 23, {Received 25 May 1972) ABBREVIATIONS INS A c epi f I m mb mf ON PLATES A-band cisternal element cuticle and epidermis fat body I-band mitochondrion myoblast myofibre mt n nv P sr t Z microtubule nucleus motor nerve myoblast process sarcoplasmic reticulum T-tubule Z-band
10 2o6 N. M. Tyrer Figs The 68 % (timed) stage. Fig. 4. Light micrograph of a i-/mn transverse section of 1 of the 4 dorsal muscles. Scale 10 fim. Fig. 5. Low-magnification electron micrograph of the muscle cut in TS in the A-band region close to the I-band. A myofibre, containing clusters of myofilaments /Jm across is seen in the centre of the field. Myofibre nuclei (n) are seen middle left and lower right and a portion of a myoblast (mb) is seen lower left. T-tubules (i) usually descend only a short distance into the fibre, but one deeply descending one is seen in the centre of the field. A few dyads (arrowed) are present. The mitochondria (m) are small, x Fig. 6. Longitudinal section of the muscle showing myofibrils 0-5 /m\ across separated by regions of sarcoplasm containing a few profiles of sarcoplasmic reticulum (sr) and some poorly oriented filaments. Mitochondria (m) occur in the I-band region. A possible dyadic association with a T-tubule is arrowed, x Fig. 7. A transverse section of the myofibre in the A-band region close to the I-band. The myofibrils are separated by sarcoplasm containing irregular, apparently swollen, elements (sr). These are interpreted as elements of sarcoplasmic reticulum which are poorly fixed. Some elements similar to these are loosely associated with the plasma membrane (cf. Kelly, 1971). A dyadic association with a short T-system element is arrowed. Note that the cisternal element (c) contains little material. The slightly corrugated appearance of the T-tubule suggests an origin similar to that of the chick (Ezerman & Ishikawa, 1967). Note the large number of thin filaments surrounding each thick filament, x
11 Development of locust SR J
12 208 N. M. Tyrer Figs The 80% stage. Fig. 8. Light micrograph of a 1 -/tm transverse section of 1 of the 4 dorsal muscles from a 77 % (timed) embryo. Note that the size of the myofibres (mf) is comparable with that of later stages (cf. Figs. 12, 16 and 20). n, myofibre nucleus. Scale 10 /an. Fig. 9. Low-magnification electron micrograph of a myofibre from the 80 % (estimated) muscle cut in TS. The myofibre is now packed with filaments. Some T-system elements (t) descend deeply into the fibre and some dyads (arrowed) are seen. Between the myofibrils are seen profiles of a sparse SR. x Fig. 10. Longitudinal section of a muscle at the 80% (estimated) stage showing some incompletely divided myofibrils between O'5 and i'o/tm in diameter. Note the long sarcomeres and irregular Z-bands. Between the myofibrils are a few profiles of sarcoplasmic reticulum (sr). Mitochondria (m) are present in the I-band region, x Fig. 11. A TS of the 77 % (timed) muscle in the A-band region close to the I-band. A sparse sarcoplasmic reticulum (sr) occurs between the myofibrils. A dyadic structure is arrowed, x
13 Development of locust SR
14 2io N.M. Tyrer Figs The 92% stage. Fig. 12. A light micrograph of a i-/im section of 1 of the 4 dorsal muscles from the 92 % (timed) stage. This micrograph shows very clearly that all the myofibres (mf) are in identical states of development. Scale 10 /tm. Fig. 13. Low-magnification electron micrograph of a myofibre in TS from a 92 % (estimated) muscle. The myofibrils are now well defined by reticular elements. T-system elements (t) descend at regular intervals from the plasma membrane. The sarcoplasmic reticulum (sr) is still sparse but dyads (arrowed) are well formed and numerous. Mitochondria (m) have more cristae than in earlier stages and some are less regular in section suggesting that they are no longer simple cylindrical structures, x Fig. 14. Longitudinal section of the muscle at the 92 % (estimated) stage. The sparse sarcoplasmic reticulum is seen between the myofibrils in the A-band region and well denned dyads (arrowed) occur close to the A-I band junction, x Fig. 15. A transverse section of the 92 % (timed) muscle in the A-band region close to the I-band showing myofibrils well defined by profiles of the sarcoplasmic reticulum. A T-tubule (t) is seen descending from the plasma membrane and in association with a cisterna to form a dyad which is very similar in organization to those of later stages (cf. Figs. 19, 23). Note the dense material between the T-tubule and the cisterna and also the dense contents of the cisterna. x
15 Development of locust SR 14-2
16 212 N.M. Tyrer Figs The 100% stage. Fig. 16. Light micrograph of a i-fim section of 1 of the 4 dorsal muscles. As in the 92% stage (Fig. 12) the myofibres (mf) are all at the same stage of differentiation. Their condensed appearance is due to stretching of the muscle. The motor nerve (nv) is seen descending into the muscle. Scale 10 /tm. Fig. 17. Low-magnification electron micrograph of a myofibre in TS. The sarcoplasmic reticulum is better defined than in the previous stage but it is still sparse. Dyads (arrowed) are similar in structure and number to the previous stage (Fig. 13) and to the next stage (Fig. 21). x Fig. 18. Longitudinal section showing the sparse sarcoplasmic reticulum between the myofibrils in the A-band region and well denned dyads (one arrowed) close to the A I band junction. Mitochondria occur in the I-band region as in the other stages, x Fig. 19. A transverse section in the A-band region close to the I-band. Elements of the sarcoplasmic reticulum can be distinguished from the T-tubules by their thinner walls. Note the periodic nature of the electron-dense material between the T-tubule and the cisterna in the dyad (arrowed). In favourable sections this periodicity is seen in the dyads in all stages from the 80 % onwards, x
17 Development of locust SR 213
18 214 N.M. Tyrer Figs The 5-day hopper. Fig. 20. Light micrograph of a 1 /tm section of 1 of the 4 dorsal muscles. The myofibres (»«/) are the same size as in the previous stages and all are at the same stage of differentiation. Scale 10 fira. Fig. 21. A low-power electron micrograph of a transverse section showing that the SR is highly developed compared with previous stages. In many places tiers of profiles are seen between the myofibrils and beneath the plasma membrane. Dyads (arrowed), however, are similar in structure and number to the 92 and 100 % stages. Note the irregular profiles of the mitochondria suggesting that they branch (cf. Hagopian, 1966). x Fig. 22. Longitudinal section. Note the development of the sarcoplasmic reticulum in the A-band region where several tiers of profiles occur between the myofibrils. The dyads (arrowed), however, are little different from the previous stages. Mitochondria are seen in the I-band region, x Fig. 23. A transverse section in the A-band close to the I-band. Note the well developed sarcoplasmic reticulum and the unchanged appearance of the cisterna (c) and the T-tubule (t). There is some indication of periodicity in the electron-dense material between the T-tubule and the cisterna. x
19 20 D/mt>JfrhmfiU.t nf Inrust SR
20
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