Advertisement
Journal Articles
Phenotypic plasticity of early myogenesis and satellite cell numbers in atlantic salmon spawning in upland and lowland tributaries of a river system
I.A. Johnston, H.A. McLay, M. Abercromby, D. Robins
Journal of Experimental Biology 2000 203: 2539-2552;

Summary

Early myogenesis was studied in the offspring of Atlantic salmon (Salmo salar L.) spawning in a lowland (Sheeoch) and an upland (Baddoch) tributary of the River Dee System, Aberdeenshire, Scotland. Eggs from each population were incubated at the simulated natural thermal regimes of each stream, which was on average 2.8 degrees C cooler for the Baddoch than for the Sheeoch. Relationships between muscle cellularity variables, the density of myonuclei and responses to temperature were investigated using multivariate statistical techniques. These revealed highly significant temperature effects (P<0.001) at hatch (H) and first feeding (FF) and significant interactions between population and temperature (P<0.001), indicating that Baddoch and Sheeoch salmon responded differently to the two temperature regimes. The total cross-sectional area of white muscle (WF.ta) at the adipose fin was relatively independent of temperature at hatch and first feeding in the Sheeoch population. In contrast, for alevins of Baddoch origin, WF.ta was 18.9% (H) and 30.5% (FF) higher in fish incubated at Baddoch than at Sheeoch temperatures. At hatch, there were 15.6% more white muscle fibres (WF.no) at the cooler incubation temperature in fish of Sheeoch origin and 6.0% more in fish of Baddoch origin. However, by first feeding, the difference in WF.no between temperatures had narrowed to 7.2% in the Sheeoch fish and increased to 17.4% in the Baddoch population. In contrast, at hatch, the density of myonuclei was 59.8% higher at the warmer incubation temperature in the Sheeoch population and 23.5% higher in the Baddoch population, but differences were less evident at first feeding. In Baddoch fish, 22.5% of the total muscle nuclei were actively dividing at first feeding, as assessed by staining for proliferating cell nuclear antigen (PCNA). Of the PCNA-positive nuclei, 78% were present in cells that stained for the c-met tyrosine kinase receptor, a marker of satellite cells and their division products. The proportion of c-met-positive cells staining for individual myogenic regulatory factors was 72.4% for the myogenic transcription factor MyoD, 76.3% for the myogenic transcription factor Myf-5, 62.1% for myogenin and 48.7% for the myogenic transcription factor Myf-6. For the Sheeoch population, there were 26.5% more c-met-expressing (P<0.01) and 23.2% more myogenic-regulatory-factor-expressing (P<0.05) cells at Sheeoch than at Baddoch temperatures. In contrast, incubation temperature had no significant effects on satellite cell density in the Baddoch population.

REFERENCES

    1. Abbott, K. L.,
    2. Friday, B. B.,
    3. Thaloor, D.,
    4. Murphy, T. J. and
    5. Pavlath, G. K.
    (1998). Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell 9, 2905–.
    OpenUrlAbstract/FREE Full Text
    1. Bravo, R.,
    2. Frank, R.,
    3. Blundell, P. A. and
    4. MacDonald-Bravo, H.
    (1987). Cyclin/PCNA is the auxillary protein of DNA polymerase-. Nature 326, 515–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Cornelison, D. D. W. and
    2. Wold, B. J.
    (1997). Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol 191, 270–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Devoto, S. H.,
    2. Melancon, E.,
    3. Eisen, J. S. and
    4. Westerfield, M.
    (1996). Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122, 3371–.
    OpenUrlAbstract
    1. Halpern, M. E.,
    2. Ho, R. K.,
    3. Walker, C. and
    4. Kimmel, C. B.
    (1993). Induction of muscle pioneers and floor plate is distinguished by the zebrafish notail mutation. Cell 75, 99–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnston, I. A.,
    2. Cole, N. J.,
    3. Abercromby, M. and
    4. Vieira, V. L. A.
    (1998). Embryonic temperature modulates muscle growth characteristics in larval and juvenile herring. J. Exp. Biol 201, 623–.
    1. Johnston, I. A. and
    2. McLay, H. A.
    (1997). Temperature and family effects on muscle cellularity at hatch and first feeding in Atlantic salmon (Salmo salar L.). Can J. Zool 75, 64–.
    OpenUrlCrossRef
    1. Johnston, I. A.,
    2. McLay, H. A.,
    3. Abercromby, M. and
    4. Robbins, D.
    (2000). Egg incubation temperature produces different effects on muscle fibre recruitment patterns in spring-and autumn-running Atlantic salmon populations. J. Exp. Biol 203, 2553–.
    OpenUrlAbstract
    1. Johnston, I. A.,
    2. Strugnell, G.,
    3. McCracken, M. L. and
    4. Jonstone, R.
    (1999). Muscle growth and development in normal-sex-ratio and all-female diploid and triploid Atlantic salmon. J. Exp. Biol 202, 1991–.
    OpenUrlAbstract
    1. Johnston, I. A.,
    2. Vieira, V. L. A. and
    3. Abercromby, M.
    (1995). 2552Temperature and myogenesis in embryos of Atlantic herring Clupea harengus. J. Exp. Biol 198, 1389–.
    OpenUrlAbstract/FREE Full Text
    1. Koumans, J. T. M. and
    2. Akster, H. A.
    (1995). Myogenic cells in development and growth of fish. Comp. Biochem. Physiol 110, 3–.
    OpenUrlCrossRef
    1. Megeney, L. A. and
    2. Rudnicki, M. A.
    (1995). Determination versus differentiation and the MyoD family of transcription factors. Biochem. Cell Biol 73, 723–.
    OpenUrlPubMedWeb of Science
    1. Musarò, A.,
    2. McCullagh, K. J. A.,
    3. Naya, F. J.,
    4. Olson, E. N. and
    5. Rosenthal, N.
    (1999). IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-Atc1. Nature 400, 581–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Semsarian, C.,
    2. Ming-Jie, W.,
    3. Yue-Kun, J.,
    4. Marciniec, T.,
    5. Yeoh, T.,
    6. Allen, D. G.,
    7. Harvey, R. P. and
    8. Graham, R. M.
    (1999). Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature 400, 576–.
    OpenUrlCrossRefPubMed
    1. Stabell, O. B.
    (1984). Homing and olfaction in salmonids: a criticalreview with special reference to Atlantic salmon. Biol. Rev 59, 333–.
    OpenUrl
    1. Stickland, N. C.,
    2. White, R. N.,
    3. Mescall, P. E.,
    4. Crook, A. R. and
    5. Thorpe, J. E.
    (1988). The effect of temperature on myogenesis in embryonic development of the Atlantic salmon (Salmo salar L.). Anat. Embryol 178, 253–.
    OpenUrlCrossRefPubMed
    1. Stoiber, W. and
    2. Sänger, A. M.
    (1996). An electron microscopic investigation into the possible source of new muscle fibres in teleost fish. Anat. Embryol 194, 569–.
    OpenUrlPubMed
    1. Tatsumi, R.,
    2. Anderson, J. E.,
    3. Nevoret, C. J.,
    4. Halevy, O. and
    5. Allen, R. E.
    (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol 194, 114–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Weinberg, E. S.,
    2. Allende, M. L.,
    3. Kelly, C. S.,
    4. Abdelhami, D. A.,
    5. Murakami, T.,
    6. Anderman, P.,
    7. Doerre, O. G.,
    8. Gunwald, D. J. and
    9. Riggleman, B.
    (1996). Developmental regulation of zebrafish MyoD in normal sex ratio, no tail and spadetail embryos. Development 122, 271–.
    OpenUrlAbstract
    1. Yablonka-Reuveni, Z.,
    2. Rudnicki, M. A.,
    3. Rivera, A. J.,
    4. Primig, M.,
    5. Anderson, J. E. and
    6. Natanson, P.
    (1999). The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev. Biol 210, 440–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Yang, Q.,
    2. Basel-Duby, R. and
    3. Williams, S. R.
    (1997). Transient expression of a winged-helix protein, MNF-, during myogenesis. Mol. Cell. Biol 17, 5236–.
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Articles
Phenotypic plasticity of early myogenesis and satellite cell numbers in atlantic salmon spawning in upland and lowland tributaries of a river system
I.A. Johnston, H.A. McLay, M. Abercromby, D. Robins
Journal of Experimental Biology 2000 203: 2539-2552;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Welcome to JEB’s new Editor Monica Daley

We are pleased to welcome Monica Daley to JEB’s Editorial team. Monica has had a long association with JEB before taking up her new role, overseeing peer review of neuromuscular physiology, terrestrial biomechanics and integrative physiology of locomotion.

In the field with Robyn Hetem

Continuing our fieldwork series, Robyn Hetem reflects on working with species ranging from aardvark to zebra, and the impact COVID-19 has had on fieldwork.

Read & Publish participation continues to grow

“It is particularly encouraging for early career researchers, as it allows them to display their research globally without the need to find costs to cover the open access option.”

Professor Fernando Montealegre-Z (University of Lincoln) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Nocturnal reef residents have deep-sea-like eyes

Fanny de Busserolles and colleagues from The University of Queensland have discovered that the eyes of nocturnal reef fish have multibank retinas, layers of photoreceptors, similar to the eyes of deep-sea fish that live in dim light conditions.

Mechanisms underlying gut microbiota–host interactions in insects

In their Review, Konstantin Schmidt and Philipp Engel summarise recent findings about the mechanisms involved in gut colonisation and the provisioning of beneficial effects in gut microbiota–insect symbiosis.