Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.

Hedgehog (Hh) genes play major roles in animal development and studies of their evolution, expression and function point to major differences among chordates. Here we focused on Hh genes in lampreys in order to characterize the evolution of Hh signalling at the emergence of vertebrates. Screening of...

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Main Authors: Shungo Kano, Jin-Hua Xiao, Joana Osório, Marc Ekker, Yavor Hadzhiev, Ferenc Müller, Didier Casane, Ghislaine Magdelenat, Sylvie Rétaux
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-10-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20967201/pdf/?tool=EBI
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spelling doaj-bb2774d9136c4d0e988713db1630a3912021-03-04T02:17:26ZengPublic Library of Science (PLoS)PLoS ONE1932-62032010-10-01510e1333210.1371/journal.pone.0013332Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.Shungo KanoJin-Hua XiaoJoana OsórioMarc EkkerYavor HadzhievFerenc MüllerDidier CasaneGhislaine MagdelenatSylvie RétauxHedgehog (Hh) genes play major roles in animal development and studies of their evolution, expression and function point to major differences among chordates. Here we focused on Hh genes in lampreys in order to characterize the evolution of Hh signalling at the emergence of vertebrates. Screening of a cosmid library of the river lamprey Lampetra fluviatilis and searching the preliminary genome assembly of the sea lamprey Petromyzon marinus indicate that lampreys have two Hh genes, named Hha and Hhb. Phylogenetic analyses suggest that Hha and Hhb are lamprey-specific paralogs closely related to Sonic/Indian Hh genes. Expression analysis indicates that Hha and Hhb are expressed in a Sonic Hh-like pattern. The two transcripts are expressed in largely overlapping but not identical domains in the lamprey embryonic brain, including a newly-described expression domain in the nasohypophyseal placode. Global alignments of genomic sequences and local alignment with known gnathostome regulatory motifs show that lamprey Hhs share conserved non-coding elements (CNE) with gnathostome Hhs albeit with sequences that have significantly diverged and dispersed. Functional assays using zebrafish embryos demonstrate gnathostome-like midline enhancer activity for CNEs contained in intron2. We conclude that lamprey Hh genes are gnathostome Shh-like in terms of expression and regulation. In addition, they show some lamprey-specific features, including duplication and structural (but not functional) changes in the intronic/regulatory sequences.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20967201/pdf/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Shungo Kano
Jin-Hua Xiao
Joana Osório
Marc Ekker
Yavor Hadzhiev
Ferenc Müller
Didier Casane
Ghislaine Magdelenat
Sylvie Rétaux
spellingShingle Shungo Kano
Jin-Hua Xiao
Joana Osório
Marc Ekker
Yavor Hadzhiev
Ferenc Müller
Didier Casane
Ghislaine Magdelenat
Sylvie Rétaux
Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
PLoS ONE
author_facet Shungo Kano
Jin-Hua Xiao
Joana Osório
Marc Ekker
Yavor Hadzhiev
Ferenc Müller
Didier Casane
Ghislaine Magdelenat
Sylvie Rétaux
author_sort Shungo Kano
title Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
title_short Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
title_full Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
title_fullStr Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
title_full_unstemmed Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs.
title_sort two lamprey hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome hedgehogs.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2010-10-01
description Hedgehog (Hh) genes play major roles in animal development and studies of their evolution, expression and function point to major differences among chordates. Here we focused on Hh genes in lampreys in order to characterize the evolution of Hh signalling at the emergence of vertebrates. Screening of a cosmid library of the river lamprey Lampetra fluviatilis and searching the preliminary genome assembly of the sea lamprey Petromyzon marinus indicate that lampreys have two Hh genes, named Hha and Hhb. Phylogenetic analyses suggest that Hha and Hhb are lamprey-specific paralogs closely related to Sonic/Indian Hh genes. Expression analysis indicates that Hha and Hhb are expressed in a Sonic Hh-like pattern. The two transcripts are expressed in largely overlapping but not identical domains in the lamprey embryonic brain, including a newly-described expression domain in the nasohypophyseal placode. Global alignments of genomic sequences and local alignment with known gnathostome regulatory motifs show that lamprey Hhs share conserved non-coding elements (CNE) with gnathostome Hhs albeit with sequences that have significantly diverged and dispersed. Functional assays using zebrafish embryos demonstrate gnathostome-like midline enhancer activity for CNEs contained in intron2. We conclude that lamprey Hh genes are gnathostome Shh-like in terms of expression and regulation. In addition, they show some lamprey-specific features, including duplication and structural (but not functional) changes in the intronic/regulatory sequences.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20967201/pdf/?tool=EBI
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