Progressive Loss of Function in a Limb Enhancer during Snake Evolution

The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major morphological transitions in vertebrates have remained elusive. We identified snake-specific sequence changes within an otherwise highly conserved long...

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Veröffentlicht in:	Cell Jg. 167; H. 3; S. 633
Hauptverfasser:	Kvon, Evgeny Z, Kamneva, Olga K, Melo, Uirá S, Barozzi, Iros, Osterwalder, Marco, Mannion, Brandon J, Tissières, Virginie, Pickle, Catherine S, Plajzer-Frick, Ingrid, Lee, Elizabeth A, Kato, Momoe, Garvin, Tyler H, Akiyama, Jennifer A, Afzal, Veena, Lopez-Rios, Javier, Rubin, Edward M, Dickel, Diane E, Pennacchio, Len A, Visel, Axel
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 20.10.2016
Schlagworte:	Animals Base Sequence Biological Evolution Enhancer Elements, Genetic Evolution, Molecular Extremities - growth & development Gene Knock-In Techniques Hedgehog Proteins - genetics Mice Mice, Transgenic Mutation Phylogeny Snakes - classification Snakes - genetics evo-devo limb development genome editing Sonic hedgehog (Shh) enhancer CRISPR/Cas9 cis-regulatory element morphological evolution ZRS snakes
ISSN:	1097-4172, 1097-4172
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Abstract	The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major morphological transitions in vertebrates have remained elusive. We identified snake-specific sequence changes within an otherwise highly conserved long-range limb enhancer of Sonic hedgehog (Shh). Transgenic mouse reporter assays revealed that the in vivo activity pattern of the enhancer is conserved across a wide range of vertebrates, including fish, but not in snakes. Genomic substitution of the mouse enhancer with its human or fish ortholog results in normal limb development. In contrast, replacement with snake orthologs caused severe limb reduction. Synthetic restoration of a single transcription factor binding site lost in the snake lineage reinstated full in vivo function to the snake enhancer. Our results demonstrate changes in a regulatory sequence associated with a major body plan transition and highlight the role of enhancers in morphological evolution. PAPERCLIP.
AbstractList	The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major morphological transitions in vertebrates have remained elusive. We identified snake-specific sequence changes within an otherwise highly conserved long-range limb enhancer of Sonic hedgehog (Shh). Transgenic mouse reporter assays revealed that the in vivo activity pattern of the enhancer is conserved across a wide range of vertebrates, including fish, but not in snakes. Genomic substitution of the mouse enhancer with its human or fish ortholog results in normal limb development. In contrast, replacement with snake orthologs caused severe limb reduction. Synthetic restoration of a single transcription factor binding site lost in the snake lineage reinstated full in vivo function to the snake enhancer. Our results demonstrate changes in a regulatory sequence associated with a major body plan transition and highlight the role of enhancers in morphological evolution. PAPERCLIP.The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major morphological transitions in vertebrates have remained elusive. We identified snake-specific sequence changes within an otherwise highly conserved long-range limb enhancer of Sonic hedgehog (Shh). Transgenic mouse reporter assays revealed that the in vivo activity pattern of the enhancer is conserved across a wide range of vertebrates, including fish, but not in snakes. Genomic substitution of the mouse enhancer with its human or fish ortholog results in normal limb development. In contrast, replacement with snake orthologs caused severe limb reduction. Synthetic restoration of a single transcription factor binding site lost in the snake lineage reinstated full in vivo function to the snake enhancer. Our results demonstrate changes in a regulatory sequence associated with a major body plan transition and highlight the role of enhancers in morphological evolution. PAPERCLIP. The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major morphological transitions in vertebrates have remained elusive. We identified snake-specific sequence changes within an otherwise highly conserved long-range limb enhancer of Sonic hedgehog (Shh). Transgenic mouse reporter assays revealed that the in vivo activity pattern of the enhancer is conserved across a wide range of vertebrates, including fish, but not in snakes. Genomic substitution of the mouse enhancer with its human or fish ortholog results in normal limb development. In contrast, replacement with snake orthologs caused severe limb reduction. Synthetic restoration of a single transcription factor binding site lost in the snake lineage reinstated full in vivo function to the snake enhancer. Our results demonstrate changes in a regulatory sequence associated with a major body plan transition and highlight the role of enhancers in morphological evolution. PAPERCLIP.
Author	Akiyama, Jennifer A Tissières, Virginie Pickle, Catherine S Afzal, Veena Osterwalder, Marco Kato, Momoe Garvin, Tyler H Kamneva, Olga K Barozzi, Iros Melo, Uirá S Mannion, Brandon J Pennacchio, Len A Lee, Elizabeth A Rubin, Edward M Dickel, Diane E Visel, Axel Kvon, Evgeny Z Plajzer-Frick, Ingrid Lopez-Rios, Javier
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Keywords	evo-devo limb development genome editing Sonic hedgehog (Shh) enhancer CRISPR/Cas9 cis-regulatory element morphological evolution ZRS snakes
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Snippet	The evolution of body shape is thought to be tightly coupled to changes in regulatory sequences, but specific molecular events associated with major...
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SubjectTerms	Animals Base Sequence Biological Evolution Enhancer Elements, Genetic Evolution, Molecular Extremities - growth & development Gene Knock-In Techniques Hedgehog Proteins - genetics Mice Mice, Transgenic Mutation Phylogeny Snakes - classification Snakes - genetics
Title	Progressive Loss of Function in a Limb Enhancer during Snake Evolution
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