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First published online December 22, 2003
Journal of Experimental Biology 207, 483-495 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00754

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Morphological and functional maturation of a skeletal muscle regulated by juvenile hormone

Uwe Rose^*

University of Ulm, Department of Neurobiology, Albert-Einstein-Allee 11, 89081 Ulm, Germany

View larger version (72K): [in a new window]   Fig. 1. The ovipositor and its muscles in female grasshoppers. (A) Lateral view showing a diagram of dorsal and ventral muscles, apodeme and valvulae. When muscles 271 and 272 contract, the dorsal and ventral valvulae open. (B) Photograph of a dissection showing a dorsal view on the ovipositor opener muscle M271 from a mature female. The tendon at the posterior insertion site appears magenta-coloured. (C) Transverse sections through the apodeme-muscle complex of an immature (<5 day), mature (>14 day) and allatectomised (–CA) female. Note increased size of muscle fibre bundles and apodeme complexity in mature females. A is adapted from Snodgrass (1935) with permission. Scale bars, 1 mm (B); 0.5 mm (C).

View larger version (42K): [in a new window]   Fig. 2. Growth of valve apodeme during maturation is largely regulated by JH. (A) Scanning electron micrographs of the valve apodeme of females from different experimental groups. Apodemes of mature animals show increased length, width and a more complex surface structure than those of immature and allatectomised females (see also Fig. 1). By contrast, apodemes from immature or precocene-treated females are rather flat with a straight and smooth appearance. (B) Size-index values (lengthxwidth) of apodemes from immature (<5 day), mature (>14 day), allatectomised (–CA) and those females injected with the JH analog methoprene (–CA, +met). Apodemal size increases considerably between the 5th and the 14th day after adult emergence. Allatectomy markedly inhibits the increase, but replacement injections with methoprene are able to significantly reverse allatectomy effects. Data are means ± S.D.; ***P<0.001. Scale bar in A, 1 mm; anterior is to the right.

View larger version (67K): [in a new window]   Fig. 3. (A) Cross-sections from dorsal opener muscle 271 reveal dramatic growth of muscles fibres during maturation (a single muscle fibre is outlined in each group for comparison). Muscle fibres from allatectomised females remain almost undeveloped. Fatty tissue (ft) is frequently observed between the fibres of allatectomised females, but not in immature or mature females. (B) Quantification of fibre growth during reproductive development. Cross-sectional area of muscle fibres increase approx. sevenfold during maturation. Allatectomy prevents fibre growth (–CA), whereas methoprene injection reinitiates growth (–CA, +met). Data are means ± S.D.; ***P<0.001. Scale bar in A, 20 µm.

View larger version (129K): [in a new window]   Fig. 4. Electron micrographs of transverse (A,D,C,F) and longitudinal (B,E) sections obtained from dorsal opener muscle 271 of immature (A–C) and mature (D–F) females. In immature females, note the presence of numerous tracheoles (Tr), small irregular myofibrils and mitochondria (M). T-tubules (T) and dyads (open arrow) occur at the level of the A-band (Ab). Multiple microtubules (Mt) are present within the sarcoplasm. Elements of the sarcoplasmic reticulum (SR) are rare and not well developed. By contrast, myofibrils of mature females appear well organised and are divided by regular chains of sarcoplasmic reticulum profiles. Comparatively large mitochondria (M) are present at the level of the I-band (Ib), adjacent to the Z-line (Z). N, nucleus. Scale bars, 0.25 µm (C,F); 0.5 µm (A,B); 1 µm (C,D).

View larger version (188K): [in a new window]   Fig. 5. Electron micrographs of opener muscle from immature (A) and allatectomised (B,C,D) females. (A,C) Overview of myofibril structure. Note the abundance of tracheoles (Tr) surrounding the myofibrils and the similarity of basic organisation and structure of muscle elements in immature and allatectomised females. (B,D) Transverse (B) and longitudinal (D) sections of muscle fibres obtained from allatectomised females reveal the presence of dyads (open arrow in B) and numerous microtubules (MT in B), almost comparable to those seen in immature female fibres (compare to Fig. 4C). However, elements of the sarcoplasmic reticulum (SR) surrounding the myofibrils and mitochondria (M) appear somewhat better organised and larger when compared to fibres of immature females. Ab, A-band; Ib, I-band; N, nucleus; Z, Z-line. Scale bars, 1 µm (A,C,D); 0.25 µm (B).

View larger version (19K): [in a new window]   Fig. 6. Contraction force and kinetics of ovipositor muscle 271 obtained from immature (<5 day), mature (>14 day, sham-op.) and allatectomised females (–CA). (A) Examples of muscle contractions from immature (left) and mature females (right), showing considerably increased forces and altered kinetics. (B) Quantification of forces exerted during twitch and tetanus (50 Hz) contractions. The twitch/tetanus ratios for all groups are shown. (C) Contraction and relaxation kinetics of single twitches. Muscles from mature females contract and relax significantly faster than those of immature and allatectomised females. Data are means ± S.D.; *P<0.05; **P<0.01;***P<0.001.

View larger version (20K): [in a new window]   Fig. 7. Modulation of ovipositor muscle contractions by proctolin or high frequency pre-stimulation. (A) Application of 10–9 mol l–1 proctolin increases contraction force in all experimental groups. (B) To test for endogenous release of proctolin, contractions evoked by control stimulations are compared with those evoked by test stimulations. Shortly before the test stimulation, a high frequency pre-stimulation (50 Hz) was applied, as shown in the inset. Pre-stimulation was intended to release endogenous proctolin from neuronal elements innervating the muscle. Significant increase of contraction forces is observed in mature females only.