Ancient deuterostome origins of vertebrate brain signalling centres

Neuroectodermal signalling centres induce and pattern many novel vertebrate brain structures but are absent, or divergent, in invertebrate chordates. This has led to the idea that signalling-centre genetic programs were first assembled in stem vertebrates and potentially drove morphological innovati...

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Veröffentlicht in:Nature (London) 2012-03, Vol.483 (7389), p.289-294
Hauptverfasser: Pani, Ariel M., Mullarkey, Erin E., Aronowicz, Jochanan, Assimacopoulos, Stavroula, Grove, Elizabeth A., Lowe, Christopher J.
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container_issue 7389
container_start_page 289
container_title Nature (London)
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creator Pani, Ariel M.
Mullarkey, Erin E.
Aronowicz, Jochanan
Assimacopoulos, Stavroula
Grove, Elizabeth A.
Lowe, Christopher J.
description Neuroectodermal signalling centres induce and pattern many novel vertebrate brain structures but are absent, or divergent, in invertebrate chordates. This has led to the idea that signalling-centre genetic programs were first assembled in stem vertebrates and potentially drove morphological innovations of the brain. However, this scenario presumes that extant cephalochordates accurately represent ancestral chordate characters, which has not been tested using close chordate outgroups. Here we report that genetic programs homologous to three vertebrate signalling centres — the anterior neural ridge, zona limitans intrathalamica and isthmic organizer — are present in the hemichordate Saccoglossus kowalevskii . Fgf8/17/18 (a single gene homologous to vertebrate Fgf8 , Fgf17 and Fgf18 ), sfrp1/5 , hh and wnt1 are expressed in vertebrate-like arrangements in hemichordate ectoderm, and homologous genetic mechanisms regulate ectodermal patterning in both animals. We propose that these genetic programs were components of an unexpectedly complex, ancient genetic regulatory scaffold for deuterostome body patterning that degenerated in amphioxus and ascidians, but was retained to pattern divergent structures in hemichordates and vertebrates. Genetic programs homologous to three vertebrate signalling centres are present in the hemichordate Saccoglossus kowalevskii and may be components of a complex, ancient genetic regulatory scaffold for deuterostome body patterning that degenerated in amphioxus and ascidians, but was retained to pattern divergent structures in hemichordates and vertebrates. Evolutionary roots of the vertebrate brain The vertebrate brain is a complex structure, and how it evolved from a simpler nervous system remains obscure. The invertebrates most closely related to vertebrates, such as sea squirts and lancelets, have very much simpler brains, and it has been widely assumed that the vertebrate brain has a uniquely vertebrate evolutionary history. But work by Christopher Lowe and colleagues now shows that the genetic program that specifies the anterior end of acorn worms — very distant relatives of vertebrates, akin to echinoderms such as starfish — is very like that of vertebrates. This means that the program for specifying the vertebrate brain started out as a more generalized routine for the development of the front end of the animal. Confusion arose because the pathways involved have been lost or highly modified in lancelets and sea squirts.
doi_str_mv 10.1038/nature10838
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This has led to the idea that signalling-centre genetic programs were first assembled in stem vertebrates and potentially drove morphological innovations of the brain. However, this scenario presumes that extant cephalochordates accurately represent ancestral chordate characters, which has not been tested using close chordate outgroups. Here we report that genetic programs homologous to three vertebrate signalling centres — the anterior neural ridge, zona limitans intrathalamica and isthmic organizer — are present in the hemichordate Saccoglossus kowalevskii . Fgf8/17/18 (a single gene homologous to vertebrate Fgf8 , Fgf17 and Fgf18 ), sfrp1/5 , hh and wnt1 are expressed in vertebrate-like arrangements in hemichordate ectoderm, and homologous genetic mechanisms regulate ectodermal patterning in both animals. We propose that these genetic programs were components of an unexpectedly complex, ancient genetic regulatory scaffold for deuterostome body patterning that degenerated in amphioxus and ascidians, but was retained to pattern divergent structures in hemichordates and vertebrates. Genetic programs homologous to three vertebrate signalling centres are present in the hemichordate Saccoglossus kowalevskii and may be components of a complex, ancient genetic regulatory scaffold for deuterostome body patterning that degenerated in amphioxus and ascidians, but was retained to pattern divergent structures in hemichordates and vertebrates. Evolutionary roots of the vertebrate brain The vertebrate brain is a complex structure, and how it evolved from a simpler nervous system remains obscure. The invertebrates most closely related to vertebrates, such as sea squirts and lancelets, have very much simpler brains, and it has been widely assumed that the vertebrate brain has a uniquely vertebrate evolutionary history. But work by Christopher Lowe and colleagues now shows that the genetic program that specifies the anterior end of acorn worms — very distant relatives of vertebrates, akin to echinoderms such as starfish — is very like that of vertebrates. This means that the program for specifying the vertebrate brain started out as a more generalized routine for the development of the front end of the animal. Confusion arose because the pathways involved have been lost or highly modified in lancelets and sea squirts.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>22422262</pmid><doi>10.1038/nature10838</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0028-0836
ispartof Nature (London), 2012-03, Vol.483 (7389), p.289-294
issn 0028-0836
1476-4687
language eng
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source MEDLINE; Nature; Alma/SFX Local Collection
subjects 631/136/334/1874
631/181
631/80/86
692/698/1688/64
Animals
Biological and medical sciences
Biological Evolution
Brain
Brain - anatomy & histology
Brain - embryology
Brain - physiology
Chordata - anatomy & histology
Chordata - embryology
Chordata - genetics
Chordata - physiology
Embryos
Fibroblast Growth Factors - metabolism
Fundamental and applied biological sciences. Psychology
Genetic aspects
Genetics of eukaryotes. Biological and molecular evolution
Hedgehog Proteins - metabolism
Hemichordates
Humanities and Social Sciences
Invertebrates
Less representative or incertae sedis groups: acanthocephala, chaetognatha, gnathostomulida, lophophoria, merostomata, mesozoa, myxozoa, nematorhyncha, pararthropoda, placozoa, priapuloidea, prochordata, pycnogonida, rotifera
Mice
Molecular weight
multidisciplinary
Origin
Physiological aspects
Science
Science (multidisciplinary)
Signal Transduction
Structure
Vertebrates
Vertebrates - anatomy & histology
Vertebrates - embryology
Vertebrates - genetics
Vertebrates - physiology
Wnt Signaling Pathway
title Ancient deuterostome origins of vertebrate brain signalling centres
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