Force Transmission between Three Tissues Controls Bipolar Planar Polarity Establishment and Morphogenesis

How tissues from different developmental origins interact to achieve coordinated morphogenesis at the level of a whole organism is a fundamental question in developmental biology. While biochemical signaling pathways controlling morphogenesis have been extensively studied [1–3], morphogenesis of epithelial tissues can also be directed by mechanotransduction pathways physically linking two tissues [4–8]. C. elegans embryonic elongation requires the coordination of three tissues: muscles, the dorsal and ventral epidermis, and the lateral epidermis. Elongation starts by cell-shape changes driven by actomyosin contractions in the lateral epidermis [9, 10]. At mid-elongation, muscles become connected to the apical surface of the dorsal and ventral epidermis by molecular tendons formed by muscle integrins, extracellular matrix, and C. elegans hemidesmosomes (CeHDs). The mechanical signal generated by the onset of muscle contractions in the antero-posterior axis from mid-elongation is translated into a biochemical pathway controlling the maturation of CeHDs in the dorsal and ventral epidermis [11]. Consistently, mutations affecting muscle contractions or molecular tendons lead to a mid-elongation arrest [12]. Here, we found that the mechanical force generated by muscle contractions and relayed by molecular tendons is transmitted by adherens junctions to lateral epidermal cells, where it establishes a newly identified bipolar planar polarity of the apical PAR module. The planar polarized PAR module is then required for actin planar organization, thus contributing to the determination of the orientation of cell-shape changes and the elongation axis of the whole embryo. This mechanotransduction pathway is therefore essential to coordinate the morphogenesis of three embryonic tissues. [Display omitted] •A mechanotransduction pathway coordinates the morphogenesis of three tissues•The mechanical signal is initiated by muscle contractions•It is transduced by molecular tendons and adherens junctions•It controls bipolar planar polarity of PAR proteins and actin and, therefore, tension orientation Gillard et al. describe a mechanotransduction signaling pathway initiated by muscle contractions that controls the establishment of bipolar planar polarity and coordinates the morphogenesis of three embryonic tissues during C. elegans embryogenesis.