Collaborative Proposal: RUI: Obliquely striated muscle: A soft-bodied invertebrate solution for tuning length-force properties to meet functional demands?

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Three types of muscle cells (smooth and the cross-striated cardiac and skeletal muscles) are well known from any introductory text, yet few biologists are familiar with obliquely striated muscles. Obliquely striated muscle cells are common in soft-bodied animals, occurring in members of at least 17 phyla, yet the implications of oblique striation for the function and performance of this important muscle type are unknown. It has been assumed for decades that oblique striation permits relatively high force output over an extraordinary range of muscle lengths. Recent work, however, suggests that the contractile properties and operating length ranges of obliquely striated muscles are very diverse, even among muscles within the same individual animal. The project will investigate the contractile properties and operating length ranges of obliquely striated muscles from diverse animals. This research is likely to reveal fundamental new principles of the structure and function of muscle that would otherwise remain obscure, and provide new insight into the diversity of function and the evolution of this fiber type. The project will provide opportunities for undergraduates, especially first-generation college students and those from underrepresented backgrounds, to gain experience in physiology, biomechanics, and science communication. In partnership with the Maine State Aquarium Discovery Center, the project will develop programs for K-12 students and the general public. The project will also impact secondary education through collaboration with the UNC Baccalaureate Education in Science and Teaching (UNC-BEST) program, which offers undergraduate Biology majors opportunities to obtain licensure as a secondary school teacher in North Carolina.Although obliquely striated muscle occurs in at least 17 animal phyla, the functional implications of this striation pattern remain unclear. Early studies suggested that oblique striation allows high force output over a much wider range of muscle lengths than possible in cross-striated muscle. Recent work, however, shows that many obliquely striated muscles are incapable of such wide operating ranges and instead, there is considerable variation in this parameter. The current understanding thus fails as a general explanation for the functional significance of oblique striation. The goal of the investigation is to test a new model, based on mathematical analysis of the geometry of the myofilament array, which suggests that oblique striation evolved to allow adjustment of the length-force relationship in animals with hydrostatic skeletons. The model predicts that the length-force relationship can be adjusted by altering the stagger angle (i.e., the degree of stagger of the myofilaments), with greater stagger resulting in a wider operating range. Measurements of length-force properties, in vivo muscle activation and length changes, and muscle fiber ultrastructure will be used to test the model predictions and assess the functional significance of oblique striation. The initial investigation will focus on the myofilament stagger and the length-force relationship of muscles in the squid Doryteuthis pealeii that vary widely in function and operating length range. In addition, muscles with similar roles and length-force relationships among select taxa that span the range of Bilaterian diversity will be studied, thus identifying structural and functional convergence in obliquely striated muscles.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.