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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Sprache:eng
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Zusammenfassung: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.
ISSN:0028-0836
1476-4687
DOI:10.1038/nature10838