Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis

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...

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Main Authors: Gilbert, S, Mullan, T, Poole, R, Woollard, A
Format: Journal article
Language:English
Published: Elsevier 2020
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author Gilbert, S
Mullan, T
Poole, R
Woollard, A
author_facet Gilbert, S
Mullan, T
Poole, R
Woollard, A
author_sort Gilbert, S
collection OXFORD
description 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.
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spelling oxford-uuid:33a81edb-f694-48de-afa8-39172c4ab8682022-03-26T13:21:24ZCaudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermisJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:33a81edb-f694-48de-afa8-39172c4ab868EnglishSymplectic Elements at OxfordElsevier2020Gilbert, SMullan, TPoole, RWoollard, AStrikingly, 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.
spellingShingle Gilbert, S
Mullan, T
Poole, R
Woollard, A
Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title_full Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title_fullStr Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title_full_unstemmed Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title_short Caudal-dependent cell positioning directs morphogenesis of the C. elegans ventral epidermis
title_sort caudal dependent cell positioning directs morphogenesis of the c elegans ventral epidermis
work_keys_str_mv AT gilberts caudaldependentcellpositioningdirectsmorphogenesisofthecelegansventralepidermis
AT mullant caudaldependentcellpositioningdirectsmorphogenesisofthecelegansventralepidermis
AT pooler caudaldependentcellpositioningdirectsmorphogenesisofthecelegansventralepidermis
AT woollarda caudaldependentcellpositioningdirectsmorphogenesisofthecelegansventralepidermis