Patterns of superficial fibre formation in the European pearlfish ( Rutilus frisii meidingeri ) provide a general template for slow muscle development in teleost fish

Abstract

The debate about the pattern of muscle formation in teleost fish has recently been heightened in the literature. Here we examine superficial muscle development in the pearlfish, a cyprinid endemic to a small area of Central Europe, and uninfluenced by economic interest and breeding. Using light and electron microscopy, histochemistry and immunohistochemistry techniques, we report that: (1) Superficial fibre precursors originate close to the notochord, are part of the same cell population as the so-called muscle pioneer cells, and are transferred laterally to end up at the surface of the myotome. (2) Superficial fibre maturation is exceptionally rapid. Structural and enzymatic functionality is attained at a time when prospective deep fibres have not passed beyond the early myotube state. This strong contrast weakens as the embryo develops. (3) Apart from the muscle pioneers, the superficial fibres appear to be capable of functioning before they receive any direct innervation, implying that signals are transferred to these fibres via cell-to-cell junctions. We suggest that the capability of rapid superficial fibre maturation is a rather general feature among teleosts and may aid pre-hatch survival under a variable environment. Our results indicate that muscle formation in teleost fish may follow a common basic pattern that is open to considerable ontogenetic and phylogenetic modification in response to habitat conditions.

Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication

“…at the level of the notochord (while other adaxial cells migrate to form the superficial layer of the myotome). Those adaxial cells which differentiate in situ form the "muscle pioneers" and probably also the horizontal myoseptum, which are later intercalated between the epaxial and hypaxial myotome (Westerfield et al 1986;Felsenfeld et al 1991;Devoto et al 1996;Stoiber et al 1998; see Langeland and Kimmel 1997 ; Fig. 2D).…”

“…SHH also enhances the formation of primary slow muscle fibres in bird somitic mesoderm (Cann et al 1999). In both bird and fish embryos, early somitic muscle cells are functional prior to innervation (Stockdale 1997;Stoiber et al 1998). …”

The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo

“…2D). A number of studies have alluded to the distinctive architecture of the contractile apparatus of teleost slow fibers (Waterman 1969;Felsenfeld et al 1990;Stoiber et al 1998). Therefore, in its capacity as a regulatory protein, Prox1 could function to modulate the expression of specific kinds of myofibril organizing components that are unique to the terminal differentiation program of the slow fibers.…”

In situhybridisation of a large repertoire of muscle-specific transcripts in fish larvae: the new superficial slow-twitch fibres exhibit characteristics of fast-twitch differentiation

“…Very often, a layer of fibres called intermediate fibres, identified on the basis of their histochemical properties, separates the slow and the fast muscle fibres. It is now well established that the embryonic formation of the superficial slow muscle fibres involves the lateral migration of adaxial cells, which flank the notochord, from the deep part of the myotome toward the lateral surface (Devoto et al, 1996;Stoiber, 1998). The fast muscle fibres of the myotomal muscle arise from non-migrating lateral presomitic cells that do not contact the notochord.…”