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Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development.

Sakamoto K, Onimaru K, Munakata K, Suda N, Tamura M, Ochi H, Tanaka M - PLoS ONE (2009)

Bottom Line: In dogfish (Scyliorhinus canicula), however, we found that Shh was transcribed late in fin development, concomitant with Hoxd13 expression.We found that the temporal shift of Shh activity altered the size of endoskeletal elements in paired fins of zebrafish and dogfish.This process may have facilitated major morphological changes in paired appendages during vertebrate limb evolution.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Nagatsuta-cho, Yokohama, Japan.

ABSTRACT
We explored the molecular mechanisms of morphological transformations of vertebrate paired fin/limb evolution by comparative gene expression profiling and functional analyses. In this study, we focused on the temporal differences of the onset of Sonic hedgehog (Shh) expression in paired appendages among different vertebrates. In limb buds of chick and mouse, Shh expression is activated as soon as there is a morphological bud, concomitant with Hoxd10 expression. In dogfish (Scyliorhinus canicula), however, we found that Shh was transcribed late in fin development, concomitant with Hoxd13 expression. We utilized zebrafish as a model to determine whether quantitative changes in hox expression alter the timing of shh expression in pectoral fins of zebrafish embryos. We found that the temporal shift of Shh activity altered the size of endoskeletal elements in paired fins of zebrafish and dogfish. Thus, a threshold level of hox expression determines the onset of shh expression, and the subsequent heterochronic shift of Shh activity can affect the size of the fin endoskeleton. This process may have facilitated major morphological changes in paired appendages during vertebrate limb evolution.

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Diagram representing the effect of Shh expression heterochrony on vertebrate paired appendage evolution.A model suggesting that the early fin buds may have acquired low levels of Hox expression by co-option of collinear Hox expression in the main body axis [53]. Changes in accumulated Hox could have led to altered onset of Shh expression, resulting in enlargement of the endoskeletal elements during fin evolution.
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pone-0005121-g006: Diagram representing the effect of Shh expression heterochrony on vertebrate paired appendage evolution.A model suggesting that the early fin buds may have acquired low levels of Hox expression by co-option of collinear Hox expression in the main body axis [53]. Changes in accumulated Hox could have led to altered onset of Shh expression, resulting in enlargement of the endoskeletal elements during fin evolution.

Mentions: Our results provide new clues for understanding the sequential events of vertebrate fin/limb evolution, especially with respect to the molecular mechanisms that change the onset of shh expression and lead to morphological changes in endoskeletal components (Fig. 6). It has been proposed that paired appendages adopted collinear expression of Hox from the main body axis concomitant with their emergence in the body wall [3], [49], [50] (Fig. 6). Our results suggest that if threshold levels of accumulated 5′ Hox transcripts were not reached, Shh expression may have been delayed or silent in ancestral fin buds. Quantitative changes in accumulated 5′ Hox may have led to altered onset of Shh expression, resulting in enlargement of endoskeletal elements during fin evolution (Fig. 6).


Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development.

Sakamoto K, Onimaru K, Munakata K, Suda N, Tamura M, Ochi H, Tanaka M - PLoS ONE (2009)

Diagram representing the effect of Shh expression heterochrony on vertebrate paired appendage evolution.A model suggesting that the early fin buds may have acquired low levels of Hox expression by co-option of collinear Hox expression in the main body axis [53]. Changes in accumulated Hox could have led to altered onset of Shh expression, resulting in enlargement of the endoskeletal elements during fin evolution.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2664896&req=5

pone-0005121-g006: Diagram representing the effect of Shh expression heterochrony on vertebrate paired appendage evolution.A model suggesting that the early fin buds may have acquired low levels of Hox expression by co-option of collinear Hox expression in the main body axis [53]. Changes in accumulated Hox could have led to altered onset of Shh expression, resulting in enlargement of the endoskeletal elements during fin evolution.
Mentions: Our results provide new clues for understanding the sequential events of vertebrate fin/limb evolution, especially with respect to the molecular mechanisms that change the onset of shh expression and lead to morphological changes in endoskeletal components (Fig. 6). It has been proposed that paired appendages adopted collinear expression of Hox from the main body axis concomitant with their emergence in the body wall [3], [49], [50] (Fig. 6). Our results suggest that if threshold levels of accumulated 5′ Hox transcripts were not reached, Shh expression may have been delayed or silent in ancestral fin buds. Quantitative changes in accumulated 5′ Hox may have led to altered onset of Shh expression, resulting in enlargement of endoskeletal elements during fin evolution (Fig. 6).

Bottom Line: In dogfish (Scyliorhinus canicula), however, we found that Shh was transcribed late in fin development, concomitant with Hoxd13 expression.We found that the temporal shift of Shh activity altered the size of endoskeletal elements in paired fins of zebrafish and dogfish.This process may have facilitated major morphological changes in paired appendages during vertebrate limb evolution.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Nagatsuta-cho, Yokohama, Japan.

ABSTRACT
We explored the molecular mechanisms of morphological transformations of vertebrate paired fin/limb evolution by comparative gene expression profiling and functional analyses. In this study, we focused on the temporal differences of the onset of Sonic hedgehog (Shh) expression in paired appendages among different vertebrates. In limb buds of chick and mouse, Shh expression is activated as soon as there is a morphological bud, concomitant with Hoxd10 expression. In dogfish (Scyliorhinus canicula), however, we found that Shh was transcribed late in fin development, concomitant with Hoxd13 expression. We utilized zebrafish as a model to determine whether quantitative changes in hox expression alter the timing of shh expression in pectoral fins of zebrafish embryos. We found that the temporal shift of Shh activity altered the size of endoskeletal elements in paired fins of zebrafish and dogfish. Thus, a threshold level of hox expression determines the onset of shh expression, and the subsequent heterochronic shift of Shh activity can affect the size of the fin endoskeleton. This process may have facilitated major morphological changes in paired appendages during vertebrate limb evolution.

Show MeSH
Related in: MedlinePlus