Abstract
Strikingly, epithelial morphogenesis remains incomplete at the end of C. elegans embryonic development; newly hatched larvae undergo extensive remodelling of their ventral epidermis during the first larval stage (L1), when newly-born epidermal cells move ventrally to complete the epidermal syncytium. Prior to this remodelling, undivided lateral seam cells produce anterior adherens junction processes that are inherited by the anterior daughter cells following an asymmetric division during L1. These adherens junction processes provide the ventral migratory route for these anterior daughters. Here, we show that these processes are perturbed in pal-1/caudal mutant animals, resulting in their inheritance by posterior, seam-fated daughters. This causes aberrant migration of seam daughter cells, disrupting the ventral epidermis. Using 4D-lineaging, we demonstrate that this larval epidermal morphogenesis defect in pal-1 mutants can be traced directly back to an initial cell positioning defect in the embryo. pal-1 expression, driven by a single intronic enhancer, is required to correctly position the seam cells in embryos such that the appropriate cell junctions support the correct migratory paths of seam daughters later in development, irrespective of their fate. Thus, during ventral epithelial remodelling in C. elegans, we show that the position of migrating cells, specified by pal-1/caudal, appears to be more important than their fate in driving morphogenesis.
Highlights
Morphogenesis is crucial to determine the final shape and function of tissues, organs and whole animals, yet the interplay between the various driving forces, such as cell migration and cell fate determination, is not well understood (Heisenberg and Solnica-Krezel, 2008; Chan et al, 2017)
Adherens junction processes are mis-polarised in pal-1 mutants, causing abnormal migration of seam cells
In animals containing the viable e2091 allele of the homeobox caudal transcription factor pal-1, we found abnormal posterior displacement of these processes in a subset of midbody seam cells (Fig. 1B)
Summary
Morphogenesis is crucial to determine the final shape and function of tissues, organs and whole animals, yet the interplay between the various driving forces, such as cell migration and cell fate determination, is not well understood (Heisenberg and Solnica-Krezel, 2008; Chan et al, 2017). These processes are always inherited by the anterior, hyp7-fated daughter, providing a migratory route for the cell towards the ventral midline to form the hyp ventral syncytium (Podbilewicz and White, 1994; Whangbo et al, 2000, see Fig. 1A) These polarised projections are unique to L1, and are not observed in seam cells later in post-embryonic development, during. We demonstrate, using 4D-lineaging, that pal-1 expression, driven by a single intronic enhancer in the same subset of epithelial cells, is required to correctly position the lateral seam cells with respect to the ventral P cells in embryos This pal-1mediated embryonic cell sorting positions adherens junctions to support the L1 ventral intercalation of only the anterior hyp epidermal daughters. The involvement of pal-1 in regulating cell movement has resonance with mammalian studies, where caudal homologues are associated with tumour metastasis involving aberrant cell migrations (Mallo et al, 1998; Chun et al, 2007; Gross et al, 2008; Li et al, 2015)
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