ABSTRACT
Specialized epithelia produce apical matrices with distinctive topographies by enigmatic mechanisms. Here, we describe a holistic mechanism that integrates cortical actomyosin dynamics with apical matrix remodeling to pattern C. elegans cuticles. Therein, axial AFBs appear near the surface of lateral epidermal syncytia during a pulse of transverse apical constriction (AC). AC generates temporary protrusions from the apical surface of epidermal syncytia, protrusions, coupled to a provisional matrix (sheath). In turn, sheath components pattern permanent ridges on the midline of adult cuticles (alae). Thus, forces generated by short-lived actin networks are relayed via the larval sheath to sculpt long-lived features of an acellular apical ECM. Further, we find that transient circumferential actin filament bundles (CFBs) in adjacent syncytia (hyp7) are largely dispensable for propagation of the annular cuticle features across development. Rather, these CFBs extend from actin bundles overlying body wall muscles and situated between known cell-ECM attachment complexes. Similar molecular and biophysical mechanisms may affect outcomes of AC and the formation of integumentary organs in higher metazoans.