A conserved Shh cis-regulatory module highlights a common developmental origin of unpaired and paired fins

Letelier, Joaquin; Calle‐Mustienes, Elisa de la; Pieretti, Joyce; Naranjo, Silvia; Maeso, Ignacio; Nakamura, Tetsuya; Pascual-Anaya, Juan; Shubin, Neil H.; Schneider, Igor; Martı́nez-Morales, Juan Ramón; Gómez-Skármeta, José Luis

doi:10.1038/s41588-018-0080-5

Cited by 79 publications

(75 citation statements)

References 41 publications

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“…One hypothesis is that these two genes could have evolved through the duplication of a Tbx4/5 gene that controlled the position of the ancestral paired fin (Agulnik et al, 1996;Hadzhiev et al, 2007;Onimaru & Kuraku, 2018;Ruvinsky & Gibson-Brown, 2000;Tanaka et al, 2002). As previously mentioned, some authors have also proposed that the origin of the paired fins can be explained by the lateral redeployment of developmental mechanisms originally associated with the median fins (Crotwell et al, 2001;Crotwell & Mabee, 2007;Freitas et al, 2014Freitas et al, , 2006Letelier et al, 2018). This hypothesis is supported by the similarities in molecular signalling pathways between developing median and paired fins (Abe et al, 2007;Freitas et al, 2014Freitas et al, , 2006.…”

Section: Discussionmentioning

confidence: 99%

A critical appraisal of appendage disparity and homology in fishes

2019

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Fishes are both extremely diverse and morphologically disparate. Part of this disparity can be observed in the numerous possible fin configurations that may differ in terms of the number of fins as well as fin shapes, sizes and relative positions on the body. Here, we thoroughly review the major patterns of disparity in fin configurations for each major group of fishes and discuss how median and paired fin homologies have been interpreted over time. When taking into account the entire span of fish diversity, including both extant and fossil taxa, the disparity in fin morphologies greatly complicates inferring homologies for individual fins. Given the phylogenetic scope of this review, structural and topological criteria appear to be the most useful indicators of fin identity. We further suggest that it may be advantageous to consider some of these fin homologies as nested within the larger framework of homologous fin‐forming morphogenetic fields. We also discuss scenarios of appendage evolution and suggest that modularity may have played a key role in appendage disparification. Fin modules re‐expressed within the boundaries of fin‐forming fields could explain how some fins may have evolved numerous times independently in separate lineages (e.g., adipose fin), or how new fins may have evolved over time (e.g., anterior and posterior dorsal fins, pectoral and pelvic fins). We favour an evolutionary scenario whereby median appendages appeared from a unique field of competence first positioned throughout the dorsal and ventral midlines, which was then redeployed laterally leading to paired appendages.

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Section: Discussionmentioning

confidence: 99%

A critical appraisal of appendage disparity and homology in fishes

2019

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“…Similarly, the genomic region around the Sonic hedgehog (Shh) gene emerged by a chromosome rearrangement at the base of the vertebrate lineage, which allowed the recruitment and incorporation of the Lmbr1 gene to the Shh TAD [3,41]. The intron 5 of Lmbr1 became a substrate for the emergence of the Shh longdistance ZRS enhancer, a critical CRE for unpaired and paired fin evolution [42]. Interestingly, a recent study investigating hindbrain boundary formation in different fish species provides a more detailed picture about the molecular events leading to novel morphological structures [43··].…”

Section: Tad Restructuring During Evolutionmentioning

confidence: 99%

An evolutionary perspective of regulatory landscape dynamics in development and disease

Franke

Gómez-Skármeta

2018

Current Opinion in Cell Biology

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The organization of animal genomes into topologically associating domains (TADs) provides a structural scaffold in which cis-regulatory elements (CREs) operate on their target genes. Determining the position of CREs and genes relative to TADs has become instrumental to trace gene expression changes during evolution and in diseases. Here we will review recent studies and discuss TADs as structural units with respect to their conservation and stability during genome reorganization. Furthermore, we describe how TAD restructuring contributed to morphological novelties during evolution but also their deleterious effects associated with disease. Despite considering TADs as structural units, the nested and dynamic scaffold within TADs contributes to tissue-specific gene expression, implying that such changes can also account for gene expression differences during evolution.

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“…The deep conservation and early stages of expression mediated by these Shh enhancers suggest a fundamental role in generating ancient, shared vertebrate characteristics. Studies to date show a modular composition of the Shh regulatory domain and thus, for at least some of the cis-regulators, there is a simple relationship of a single enhancer to a distinct spatial domain of expression (Jeong et al, 2006;Lettice et al, 2014); although, in other instances, secondary enhancers provide compensatory low levels of expression (Letelier et al, 2018;Tsukiji et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

A Highly ConservedShhEnhancer Coordinates Hypothalamic and Craniofacial Development

Crane-Smith

Schoenebeck

Graham

et al. 2019

Preprint

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Enhancers that are conserved deep in evolutionary time regulate characteristics held in common across taxonomic classes. Here, we deleted the highly conserved Shh enhancer SBE2 (Shh brain enhancer 2) which markedly reduced expression within the embryonic brain specifically in the rostral diencephalon; however, a putative secondary enhancer driving low levels of Shh partially compensated for the loss of SBE2. Further reduction of Shh levels, crossing the SBE2 deletion with the Shh null allele, disrupted brain and craniofacial tissue, linking SBE2 regulated expression to multiple defects and enabling analysis of development at different expression levels. Development of the hypothalamus, derived from the rostral diencephalon, was disrupted along both the anterior-posterior (AP) and the dorsal-ventral (DV) axes. DV patterning was highly sensitive to Shh expression levels, demonstrating a novel morphogenic context forShh. In addition, loss of SBE2 activity in the diencephalon disrupted neighbouring craniofacial development, including the mediolateral patterning of the bones along the cranial floor and viscerocranium. Thus, SHH signalling coordinates hypothalamic morphogenesis with the formation of the adjacent midline cranial bones that consequently protects the neural tissue.

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A conserved Shh cis-regulatory module highlights a common developmental origin of unpaired and paired fins

Cited by 79 publications

References 41 publications

A critical appraisal of appendage disparity and homology in fishes

A critical appraisal of appendage disparity and homology in fishes

An evolutionary perspective of regulatory landscape dynamics in development and disease

A Highly ConservedShhEnhancer Coordinates Hypothalamic and Craniofacial Development

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