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A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the...

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Autores principales: Janssen, Ralf, Pechmann, Matthias, Turetzek, Natascha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579682/
https://www.ncbi.nlm.nih.gov/pubmed/34753512
http://dx.doi.org/10.1186/s13227-021-00182-1
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author Janssen, Ralf
Pechmann, Matthias
Turetzek, Natascha
author_facet Janssen, Ralf
Pechmann, Matthias
Turetzek, Natascha
author_sort Janssen, Ralf
collection PubMed
description The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13227-021-00182-1.
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spelling pubmed-85796822021-11-10 A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning Janssen, Ralf Pechmann, Matthias Turetzek, Natascha EvoDevo Research The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13227-021-00182-1. BioMed Central 2021-11-09 /pmc/articles/PMC8579682/ /pubmed/34753512 http://dx.doi.org/10.1186/s13227-021-00182-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Janssen, Ralf
Pechmann, Matthias
Turetzek, Natascha
A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title_full A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title_fullStr A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title_full_unstemmed A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title_short A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning
title_sort chelicerate wnt gene expression atlas: novel insights into the complexity of arthropod wnt-patterning
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579682/
https://www.ncbi.nlm.nih.gov/pubmed/34753512
http://dx.doi.org/10.1186/s13227-021-00182-1
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