An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates
Background. Hedgehog signalling, interpreted in receiving cells by Gli transcription factors, plays a central role in the development of vertebrate and Drosphila embryos. Many aspects of the signalling pathway are conserved between these lineages, however vertebrates have diverged in at least one ke...
Hlavní autoři: | , , , |
---|---|
Médium: | Journal article |
Jazyk: | English |
Vydáno: |
Public Library of Science
2007
|
Témata: |
_version_ | 1826286463943180288 |
---|---|
author | Shimeld, S van den Heuvel, M Dawber, R Briscoe, J |
author_facet | Shimeld, S van den Heuvel, M Dawber, R Briscoe, J |
author_sort | Shimeld, S |
collection | OXFORD |
description | Background. Hedgehog signalling, interpreted in receiving cells by Gli transcription factors, plays a central role in the development of vertebrate and Drosphila embryos. Many aspects of the signalling pathway are conserved between these lineages, however vertebrates have diverged in at least one key aspect: they have evolved multiple Gli genes encoding functionally-distinct proteins, increasing the complexity of the hedgehog-dependent transcriptional response. Amphioxus is one of the closest living relatives of the vertebrates, having split from the vertebrate lineage prior to the widespread gene duplication prominent in early vertebrate evolution. Principal findings. We show that amphioxus has a single Gli gene, which is deployed in tissues adjacent to sources of hedgehog signalling derived from the midline and anterior endoderm. This shows the duplication and divergence of the Gli family, and hence the origin of vertebrate Gli functional diversity, was specific to the vertebrate lineage. However we also show that the single amphioxus Gli gene produces two distinct transcripts encoding different proteins. We utilise three tests of Gli function to examine the transcription regulatory capacities of these different proteins, demonstrating one has activating activity similar to Gli2, while the other acts as a weak repressor, similar to Gli3. Conclusions. These data show that the vertebrates and amphioxus have evolved functionally-similar repertoires of Gli proteins using parallel molecular routes; vertebrates via gene duplication and divergence, and amphioxus via alternate splicing of a single gene. Our results demonstrate that similar functional complexity of intercellular signalling can be achieved via different evolutionary pathways. |
first_indexed | 2024-03-07T01:44:10Z |
format | Journal article |
id | oxford-uuid:97da7dfb-0723-4d3d-961b-122b1703fe55 |
institution | University of Oxford |
language | English |
last_indexed | 2024-03-07T01:44:10Z |
publishDate | 2007 |
publisher | Public Library of Science |
record_format | dspace |
spelling | oxford-uuid:97da7dfb-0723-4d3d-961b-122b1703fe552022-03-27T00:02:49ZAn amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordatesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:97da7dfb-0723-4d3d-961b-122b1703fe55Zoological sciencesGenetics (medical sciences)Evolution (zoology)EnglishOxford University Research Archive - ValetPublic Library of Science2007Shimeld, Svan den Heuvel, MDawber, RBriscoe, JBackground. Hedgehog signalling, interpreted in receiving cells by Gli transcription factors, plays a central role in the development of vertebrate and Drosphila embryos. Many aspects of the signalling pathway are conserved between these lineages, however vertebrates have diverged in at least one key aspect: they have evolved multiple Gli genes encoding functionally-distinct proteins, increasing the complexity of the hedgehog-dependent transcriptional response. Amphioxus is one of the closest living relatives of the vertebrates, having split from the vertebrate lineage prior to the widespread gene duplication prominent in early vertebrate evolution. Principal findings. We show that amphioxus has a single Gli gene, which is deployed in tissues adjacent to sources of hedgehog signalling derived from the midline and anterior endoderm. This shows the duplication and divergence of the Gli family, and hence the origin of vertebrate Gli functional diversity, was specific to the vertebrate lineage. However we also show that the single amphioxus Gli gene produces two distinct transcripts encoding different proteins. We utilise three tests of Gli function to examine the transcription regulatory capacities of these different proteins, demonstrating one has activating activity similar to Gli2, while the other acts as a weak repressor, similar to Gli3. Conclusions. These data show that the vertebrates and amphioxus have evolved functionally-similar repertoires of Gli proteins using parallel molecular routes; vertebrates via gene duplication and divergence, and amphioxus via alternate splicing of a single gene. Our results demonstrate that similar functional complexity of intercellular signalling can be achieved via different evolutionary pathways. |
spellingShingle | Zoological sciences Genetics (medical sciences) Evolution (zoology) Shimeld, S van den Heuvel, M Dawber, R Briscoe, J An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title | An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title_full | An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title_fullStr | An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title_full_unstemmed | An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title_short | An amphioxus Gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
title_sort | amphioxus gli gene reveals conservation of midline patterning and the evolution of hedgehog signalling diversity in chordates |
topic | Zoological sciences Genetics (medical sciences) Evolution (zoology) |
work_keys_str_mv | AT shimelds anamphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT vandenheuvelm anamphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT dawberr anamphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT briscoej anamphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT shimelds amphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT vandenheuvelm amphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT dawberr amphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates AT briscoej amphioxusgligenerevealsconservationofmidlinepatterningandtheevolutionofhedgehogsignallingdiversityinchordates |