Nitric Oxide regulates mouth development in amphioxus

Abstract The development of the mouth in animals has fascinated researchers for decades, and a recent study proposed the modern view of recurrent evolution of protostomy and deuterostomy. Here we expanded our knowledge about conserved traits of mouth formation in chordates, testing the hypothesis th...

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Main Authors: Giovanni Annona, Filomena Caccavale, Juan Pascual-Anaya, Shigeru Kuratani, Pasquale De Luca, Anna Palumbo, Salvatore D’Aniello
Format: Article
Language:English
Published: Nature Portfolio 2017-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-08157-w
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author Giovanni Annona
Filomena Caccavale
Juan Pascual-Anaya
Shigeru Kuratani
Pasquale De Luca
Anna Palumbo
Salvatore D’Aniello
author_facet Giovanni Annona
Filomena Caccavale
Juan Pascual-Anaya
Shigeru Kuratani
Pasquale De Luca
Anna Palumbo
Salvatore D’Aniello
author_sort Giovanni Annona
collection DOAJ
description Abstract The development of the mouth in animals has fascinated researchers for decades, and a recent study proposed the modern view of recurrent evolution of protostomy and deuterostomy. Here we expanded our knowledge about conserved traits of mouth formation in chordates, testing the hypothesis that nitric oxide (NO) is a potential regulator of this process. In the present work we show for the first time that NO is an essential cell signaling molecule for cephalochordate mouth formation, as previously shown for vertebrates, indicating its conserved ancestral role in chordates. The experimental decrease of NO during early amphioxus Branchiostoma lanceolatum development impaired the formation of the mouth and gill slits, demonstrating that it is a prerequisite in pharyngeal morphogenesis. Our results represent the first step in the understanding of NO physiology in non-vertebrate chordates, opening new evolutionary perspectives into the ancestral importance of NO homeostasis and acquisition of novel biological roles during evolution.
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spelling doaj.art-9de11b66dcdc4b5ebca123017304a2612022-12-21T21:19:40ZengNature PortfolioScientific Reports2045-23222017-08-017111010.1038/s41598-017-08157-wNitric Oxide regulates mouth development in amphioxusGiovanni Annona0Filomena Caccavale1Juan Pascual-Anaya2Shigeru Kuratani3Pasquale De Luca4Anna Palumbo5Salvatore D’Aniello6Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn di NapoliBiology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn di NapoliEvolutionary Morphology Laboratory, RIKENEvolutionary Morphology Laboratory, RIKENRIMAR, Stazione Zoologica Anton Dohrn di NapoliBiology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn di NapoliBiology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn di NapoliAbstract The development of the mouth in animals has fascinated researchers for decades, and a recent study proposed the modern view of recurrent evolution of protostomy and deuterostomy. Here we expanded our knowledge about conserved traits of mouth formation in chordates, testing the hypothesis that nitric oxide (NO) is a potential regulator of this process. In the present work we show for the first time that NO is an essential cell signaling molecule for cephalochordate mouth formation, as previously shown for vertebrates, indicating its conserved ancestral role in chordates. The experimental decrease of NO during early amphioxus Branchiostoma lanceolatum development impaired the formation of the mouth and gill slits, demonstrating that it is a prerequisite in pharyngeal morphogenesis. Our results represent the first step in the understanding of NO physiology in non-vertebrate chordates, opening new evolutionary perspectives into the ancestral importance of NO homeostasis and acquisition of novel biological roles during evolution.https://doi.org/10.1038/s41598-017-08157-w
spellingShingle Giovanni Annona
Filomena Caccavale
Juan Pascual-Anaya
Shigeru Kuratani
Pasquale De Luca
Anna Palumbo
Salvatore D’Aniello
Nitric Oxide regulates mouth development in amphioxus
Scientific Reports
title Nitric Oxide regulates mouth development in amphioxus
title_full Nitric Oxide regulates mouth development in amphioxus
title_fullStr Nitric Oxide regulates mouth development in amphioxus
title_full_unstemmed Nitric Oxide regulates mouth development in amphioxus
title_short Nitric Oxide regulates mouth development in amphioxus
title_sort nitric oxide regulates mouth development in amphioxus
url https://doi.org/10.1038/s41598-017-08157-w
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AT filomenacaccavale nitricoxideregulatesmouthdevelopmentinamphioxus
AT juanpascualanaya nitricoxideregulatesmouthdevelopmentinamphioxus
AT shigerukuratani nitricoxideregulatesmouthdevelopmentinamphioxus
AT pasqualedeluca nitricoxideregulatesmouthdevelopmentinamphioxus
AT annapalumbo nitricoxideregulatesmouthdevelopmentinamphioxus
AT salvatoredaniello nitricoxideregulatesmouthdevelopmentinamphioxus