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Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics

BACKGROUND: The morphogenesis of the shell field is an essential step of molluscan shell formation, which exhibits both conserved features and interlineage variations. As one major gastropod lineage, the patellogastropods show different characters in its shell field morphogenesis compared to other g...

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Autores principales: Yang, Weihong, Huan, Pin, Liu, Baozhong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439683/
https://www.ncbi.nlm.nih.gov/pubmed/32814562
http://dx.doi.org/10.1186/s12861-020-00223-3
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author Yang, Weihong
Huan, Pin
Liu, Baozhong
author_facet Yang, Weihong
Huan, Pin
Liu, Baozhong
author_sort Yang, Weihong
collection PubMed
description BACKGROUND: The morphogenesis of the shell field is an essential step of molluscan shell formation, which exhibits both conserved features and interlineage variations. As one major gastropod lineage, the patellogastropods show different characters in its shell field morphogenesis compared to other gastropods (e.g., the pulmonate gastropod Lymnaea stagnalis), likely related to its epibolic gastrulation. The investigation on the shell field morphogenesis of patellogastropods would be useful to reveal the lineage-specific characters in the process and explore the deep conservation among different molluscan lineages. RESULTS: We investigated the early shell field morphogenesis in the patellogastropod Lottia goshimai using multiple techniques. Electron microscopy revealed distinct morphological characters for the central and peripheral cells of the characteristic rosette-like shell field. Gene expression analysis and F-actin staining suggested that the shell field morphogenesis in this species predominantly relied on cell movement and F-actin dynamics, while BrdU assay revealed that cell proliferation contributed little to the process. We found constant contacts between ectodermal and meso/endodermal tissues during the early stages of shell field morphogenesis, which did not support the induction of shell field by endodermal tissues in general, but a potential stage-specific induction was indicated. CONCLUSIONS: Our results emphasize the roles of cell movement and F-actin dynamics during the morphogenesis of the shell field in Lo. goshimai, and suggest potential regulators such as diffusible factors and F-actin modulators. These findings reflect the differences in shell field morphogenesis of different gastropods, and add to the knowledge of molluscan larval shell formation.
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spelling pubmed-74396832020-08-24 Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics Yang, Weihong Huan, Pin Liu, Baozhong BMC Dev Biol Research Article BACKGROUND: The morphogenesis of the shell field is an essential step of molluscan shell formation, which exhibits both conserved features and interlineage variations. As one major gastropod lineage, the patellogastropods show different characters in its shell field morphogenesis compared to other gastropods (e.g., the pulmonate gastropod Lymnaea stagnalis), likely related to its epibolic gastrulation. The investigation on the shell field morphogenesis of patellogastropods would be useful to reveal the lineage-specific characters in the process and explore the deep conservation among different molluscan lineages. RESULTS: We investigated the early shell field morphogenesis in the patellogastropod Lottia goshimai using multiple techniques. Electron microscopy revealed distinct morphological characters for the central and peripheral cells of the characteristic rosette-like shell field. Gene expression analysis and F-actin staining suggested that the shell field morphogenesis in this species predominantly relied on cell movement and F-actin dynamics, while BrdU assay revealed that cell proliferation contributed little to the process. We found constant contacts between ectodermal and meso/endodermal tissues during the early stages of shell field morphogenesis, which did not support the induction of shell field by endodermal tissues in general, but a potential stage-specific induction was indicated. CONCLUSIONS: Our results emphasize the roles of cell movement and F-actin dynamics during the morphogenesis of the shell field in Lo. goshimai, and suggest potential regulators such as diffusible factors and F-actin modulators. These findings reflect the differences in shell field morphogenesis of different gastropods, and add to the knowledge of molluscan larval shell formation. BioMed Central 2020-08-19 /pmc/articles/PMC7439683/ /pubmed/32814562 http://dx.doi.org/10.1186/s12861-020-00223-3 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yang, Weihong
Huan, Pin
Liu, Baozhong
Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title_full Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title_fullStr Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title_full_unstemmed Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title_short Early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and F-actin dynamics
title_sort early shell field morphogenesis of a patellogastropod mollusk predominantly relies on cell movement and f-actin dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439683/
https://www.ncbi.nlm.nih.gov/pubmed/32814562
http://dx.doi.org/10.1186/s12861-020-00223-3
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