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FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish

BACKGROUND: Catfish (Siluriformes) are characterized by unique morphologies, including enlarged jaws with movable barbels and taste buds covering the entire body surface. Evolution of these characteristics was a crucial step in their adaptive radiation to freshwater environments. However, the develo...

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Autores principales: Itoyama, Tatsuya, Fukui, Makiko, Kawaguchi, Masahumi, Kaneko, Saki, Sugahara, Fumiaki, Murakami, Yasunori
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6570838/
https://www.ncbi.nlm.nih.gov/pubmed/31223485
http://dx.doi.org/10.1186/s40851-019-0135-1
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author Itoyama, Tatsuya
Fukui, Makiko
Kawaguchi, Masahumi
Kaneko, Saki
Sugahara, Fumiaki
Murakami, Yasunori
author_facet Itoyama, Tatsuya
Fukui, Makiko
Kawaguchi, Masahumi
Kaneko, Saki
Sugahara, Fumiaki
Murakami, Yasunori
author_sort Itoyama, Tatsuya
collection PubMed
description BACKGROUND: Catfish (Siluriformes) are characterized by unique morphologies, including enlarged jaws with movable barbels and taste buds covering the entire body surface. Evolution of these characteristics was a crucial step in their adaptive radiation to freshwater environments. However, the developmental processes of the catfish craniofacial region and taste buds remain to be elucidated; moreover, little is known about the molecular mechanisms underlying the morphogenesis of these structures. RESULTS: In Amur catfish (Silurus asotus), three pairs of barbel primordia are formed by 2 days post-fertilization (dpf). Innervation of the peripheral nerves and formation of muscle precursors are also established during early development. Taste buds from the oral region to the body trunk are formed by 4 dpf. We then isolated catfish cognates Shh (SaShh) and Fgf8 (SaFgf8), which are expressed in maxillary barbel primordium at 1–2 dpf. Further, SHH signal inhibition induces reduction of mandibular barbels with abnormal morphology of skeletal elements, whereas it causes no apparent abnormality in the trigeminal and facial nerve morphology. We also found that mandibular barbel lengths and number of taste buds are reduced by FGF inhibition, as seen in SHH signal inhibition. However, unlike with SHH inhibition, the abnormal morphology of the trigeminal and facial nerves was observed in FGF signal-inhibited embryos. CONCLUSION: The developmental processes of Amur catfish are consistent with those reported for other catfish species. Thus, developmental aspects of craniofacial structures and taste buds may be conserved in Siluriformes. Our findings also suggest that SHH signaling plays a crucial role in the formation of barbels and taste buds, without affecting nerve projection, while FGF signaling is required for the development of barbels, taste buds, and branchial nerves. Thus, SHH and FGF signaling plays key roles in the ontogenesis and evolution of some catfish-specific characteristics. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-019-0135-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-65708382019-06-20 FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish Itoyama, Tatsuya Fukui, Makiko Kawaguchi, Masahumi Kaneko, Saki Sugahara, Fumiaki Murakami, Yasunori Zoological Lett Research Article BACKGROUND: Catfish (Siluriformes) are characterized by unique morphologies, including enlarged jaws with movable barbels and taste buds covering the entire body surface. Evolution of these characteristics was a crucial step in their adaptive radiation to freshwater environments. However, the developmental processes of the catfish craniofacial region and taste buds remain to be elucidated; moreover, little is known about the molecular mechanisms underlying the morphogenesis of these structures. RESULTS: In Amur catfish (Silurus asotus), three pairs of barbel primordia are formed by 2 days post-fertilization (dpf). Innervation of the peripheral nerves and formation of muscle precursors are also established during early development. Taste buds from the oral region to the body trunk are formed by 4 dpf. We then isolated catfish cognates Shh (SaShh) and Fgf8 (SaFgf8), which are expressed in maxillary barbel primordium at 1–2 dpf. Further, SHH signal inhibition induces reduction of mandibular barbels with abnormal morphology of skeletal elements, whereas it causes no apparent abnormality in the trigeminal and facial nerve morphology. We also found that mandibular barbel lengths and number of taste buds are reduced by FGF inhibition, as seen in SHH signal inhibition. However, unlike with SHH inhibition, the abnormal morphology of the trigeminal and facial nerves was observed in FGF signal-inhibited embryos. CONCLUSION: The developmental processes of Amur catfish are consistent with those reported for other catfish species. Thus, developmental aspects of craniofacial structures and taste buds may be conserved in Siluriformes. Our findings also suggest that SHH signaling plays a crucial role in the formation of barbels and taste buds, without affecting nerve projection, while FGF signaling is required for the development of barbels, taste buds, and branchial nerves. Thus, SHH and FGF signaling plays key roles in the ontogenesis and evolution of some catfish-specific characteristics. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-019-0135-1) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-14 /pmc/articles/PMC6570838/ /pubmed/31223485 http://dx.doi.org/10.1186/s40851-019-0135-1 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Itoyama, Tatsuya
Fukui, Makiko
Kawaguchi, Masahumi
Kaneko, Saki
Sugahara, Fumiaki
Murakami, Yasunori
FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title_full FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title_fullStr FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title_full_unstemmed FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title_short FGF- and SHH-based molecular signals regulate barbel and craniofacial development in catfish
title_sort fgf- and shh-based molecular signals regulate barbel and craniofacial development in catfish
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6570838/
https://www.ncbi.nlm.nih.gov/pubmed/31223485
http://dx.doi.org/10.1186/s40851-019-0135-1
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