Mechanical significance of obliquely striated architecture in nematode muscle.

Abstract

In certain invertebrate muscles, adjacent narrow columns of sarcomeres are displaced along the fiber axis, providing an obliquely striated myofilament pattern in certain section planes. Although this architecture is described in many phyla and has been the subject of much discussion (1-12), its mechanical significance has yet to be resolved. In nematodes, where ultrastructural details of the obliquely striated muscle have long been known (12-19), another unique and prominent feature is the attachment of every sarcomere to the plasmalemma and basal lamina via dense bodies (Z-disc analogs). Unfortunately, the importance of this feature to the transmission of the contractile force to the cuticle is not understood outside the Caenorhabditis elegans literature: it was overlooked in recent reviews covering obliquely striated muscle (9-11). Here we consider transmission of force and oblique striation together. We compare the contractile architecture in C. elegans with that in the more complex muscle type of larger nematodes. Both types are designed to transmit the force of contraction laterally to the cuticle rather than longitudinally to the muscle ends. In the second type, folding of the contractile structure around an inward extension of the basal lamina enables a higher number of sarcomeres to be linked to cuticle per unit length. We suggest that the mechanical significance of the oblique arrangement of sarcomeres in both types is that it distributes the force application sites of the sarcomeres more evenly over the basal lamina and cuticle. With this muscle architecture, smooth bending of the nematode body tube would be possible, and kinking would be prevented.