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Biphasic Hoxd gene expression in shark paired fins reveals an ancient origin of the distal limb domain.

Freitas R, Zhang G, Cohn MJ - PLoS ONE (2007)

Bottom Line: Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods.The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans.We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Cancer/Genetics Research Complex, University of Florida, Gainesville, Florida, United Sates of America.

ABSTRACT
The evolutionary transition of fins to limbs involved development of a new suite of distal skeletal structures, the digits. During tetrapod limb development, genes at the 5' end of the HoxD cluster are expressed in two spatiotemporally distinct phases. In the first phase, Hoxd9-13 are activated sequentially and form nested domains along the anteroposterior axis of the limb. This initial phase patterns the limb from its proximal limit to the middle of the forearm. Later in development, a second wave of transcription results in 5' HoxD gene expression along the distal end of the limb bud, which regulates formation of digits. Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods. Here we test this hypothesis by investigating Hoxd gene expression during paired fin development in the shark Scyliorhinus canicula, a member of the most basal lineage of jawed vertebrates. We report that at early stages, 5'Hoxd genes are expressed in anteroposteriorly nested patterns, consistent with the initial wave of Hoxd transcription in teleost and tetrapod paired appendages. Unexpectedly, a second phase of expression occurs at later stages of shark fin development, in which Hoxd12 and Hoxd13 are re-expressed along the distal margin of the fin buds. This second phase is similar to that observed in tetrapod limbs. The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans. We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.

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Expression of Hoxd genes in catshark pectoral fins.Stages of development indicated in lower right corners of each panel. (A–D) Whole mount in situ hybridizations showing expression of Hoxd9 (A), Hoxd10 (B), Hoxd12 (C) and Hoxd13 (D). Pect, Pectoral fin bud; Cl, cloaca. Note anterior expansion of Hoxd12 and Hoxd13 in distal fin at stage 32. Arrows mark anterior limits of expression. Yellow dotted lines in the left column mark the anterior boundaries of expression at stage 22.
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pone-0000754-g002: Expression of Hoxd genes in catshark pectoral fins.Stages of development indicated in lower right corners of each panel. (A–D) Whole mount in situ hybridizations showing expression of Hoxd9 (A), Hoxd10 (B), Hoxd12 (C) and Hoxd13 (D). Pect, Pectoral fin bud; Cl, cloaca. Note anterior expansion of Hoxd12 and Hoxd13 in distal fin at stage 32. Arrows mark anterior limits of expression. Yellow dotted lines in the left column mark the anterior boundaries of expression at stage 22.

Mentions: In light of the primitive morphological characters present in shark pectoral fins [43], and our finding that development of the fin skeleton in shark embryos is strikingly different to that of zebrafish, we reasoned that the dynamics of Hoxd gene expression in shark paired fins may provide insights into the patterns that operated in the common ancestor of chondrichthyans and osteichthyans. We therefore examined Hoxd9-13 expression during development of catshark pectoral and pelvic appendages. At early stages of pectoral fin budding, Hoxd genes were expressed in collinear, nested domains along the trunk, with the most anteriorly-expressed gene, Hoxd9, marking the posterior limit of the emerging pectoral fins (Fig. 2A, stage 22). Hoxd10 extended up to the level of the mid-flank, between the pectoral and the pelvic fin regions (Fig. 2B, stage 22). Both genes were expressed in the region of the prospective pelvic fins, on either side of the cloacal region (Fig. 2A, B and Fig. 3A,B, stage 22). At the same stage, Hoxd12 was detected in the tail bud and cloacal regions (Fig. 2C and Fig. 3C), and Hoxd13 was expressed further posteriorly in both of these domains (Fig. 2D and Fig. 3D). As the pectoral fin buds became dorsoventrally flattened, Hoxd9 expression extended anteriorly throughout the fin mesenchyme, terminating at the anterior margin of the fin by stage 27 (Fig. 2A). Hoxd10 was detectable in the pectoral fins beginning at stage 26 (Fig. 2B). The Hoxd10 expression domain continued to spread anteriorly, however its anterior limit remained posterior to that of Hoxd9 (compare Fig. 2A with 2B). Hoxd12 expression appeared in the posterior region of the pectoral fin bud between stages 27 and 28, and encompassed the posterior radials at stage 29 (Fig. 2C). Hoxd13 transcripts were not detectable in the pectoral fin bud before stage 29 (Fig. 2D). The results show that during early development of catshark pectoral fins, Hoxd genes are activated in a spatially and temporally collinear pattern that resembles the first phase of Hoxd expression in tetrapod limbs and teleost fins.


Biphasic Hoxd gene expression in shark paired fins reveals an ancient origin of the distal limb domain.

Freitas R, Zhang G, Cohn MJ - PLoS ONE (2007)

Expression of Hoxd genes in catshark pectoral fins.Stages of development indicated in lower right corners of each panel. (A–D) Whole mount in situ hybridizations showing expression of Hoxd9 (A), Hoxd10 (B), Hoxd12 (C) and Hoxd13 (D). Pect, Pectoral fin bud; Cl, cloaca. Note anterior expansion of Hoxd12 and Hoxd13 in distal fin at stage 32. Arrows mark anterior limits of expression. Yellow dotted lines in the left column mark the anterior boundaries of expression at stage 22.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1937022&req=5

pone-0000754-g002: Expression of Hoxd genes in catshark pectoral fins.Stages of development indicated in lower right corners of each panel. (A–D) Whole mount in situ hybridizations showing expression of Hoxd9 (A), Hoxd10 (B), Hoxd12 (C) and Hoxd13 (D). Pect, Pectoral fin bud; Cl, cloaca. Note anterior expansion of Hoxd12 and Hoxd13 in distal fin at stage 32. Arrows mark anterior limits of expression. Yellow dotted lines in the left column mark the anterior boundaries of expression at stage 22.
Mentions: In light of the primitive morphological characters present in shark pectoral fins [43], and our finding that development of the fin skeleton in shark embryos is strikingly different to that of zebrafish, we reasoned that the dynamics of Hoxd gene expression in shark paired fins may provide insights into the patterns that operated in the common ancestor of chondrichthyans and osteichthyans. We therefore examined Hoxd9-13 expression during development of catshark pectoral and pelvic appendages. At early stages of pectoral fin budding, Hoxd genes were expressed in collinear, nested domains along the trunk, with the most anteriorly-expressed gene, Hoxd9, marking the posterior limit of the emerging pectoral fins (Fig. 2A, stage 22). Hoxd10 extended up to the level of the mid-flank, between the pectoral and the pelvic fin regions (Fig. 2B, stage 22). Both genes were expressed in the region of the prospective pelvic fins, on either side of the cloacal region (Fig. 2A, B and Fig. 3A,B, stage 22). At the same stage, Hoxd12 was detected in the tail bud and cloacal regions (Fig. 2C and Fig. 3C), and Hoxd13 was expressed further posteriorly in both of these domains (Fig. 2D and Fig. 3D). As the pectoral fin buds became dorsoventrally flattened, Hoxd9 expression extended anteriorly throughout the fin mesenchyme, terminating at the anterior margin of the fin by stage 27 (Fig. 2A). Hoxd10 was detectable in the pectoral fins beginning at stage 26 (Fig. 2B). The Hoxd10 expression domain continued to spread anteriorly, however its anterior limit remained posterior to that of Hoxd9 (compare Fig. 2A with 2B). Hoxd12 expression appeared in the posterior region of the pectoral fin bud between stages 27 and 28, and encompassed the posterior radials at stage 29 (Fig. 2C). Hoxd13 transcripts were not detectable in the pectoral fin bud before stage 29 (Fig. 2D). The results show that during early development of catshark pectoral fins, Hoxd genes are activated in a spatially and temporally collinear pattern that resembles the first phase of Hoxd expression in tetrapod limbs and teleost fins.

Bottom Line: Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods.The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans.We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Cancer/Genetics Research Complex, University of Florida, Gainesville, Florida, United Sates of America.

ABSTRACT
The evolutionary transition of fins to limbs involved development of a new suite of distal skeletal structures, the digits. During tetrapod limb development, genes at the 5' end of the HoxD cluster are expressed in two spatiotemporally distinct phases. In the first phase, Hoxd9-13 are activated sequentially and form nested domains along the anteroposterior axis of the limb. This initial phase patterns the limb from its proximal limit to the middle of the forearm. Later in development, a second wave of transcription results in 5' HoxD gene expression along the distal end of the limb bud, which regulates formation of digits. Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods. Here we test this hypothesis by investigating Hoxd gene expression during paired fin development in the shark Scyliorhinus canicula, a member of the most basal lineage of jawed vertebrates. We report that at early stages, 5'Hoxd genes are expressed in anteroposteriorly nested patterns, consistent with the initial wave of Hoxd transcription in teleost and tetrapod paired appendages. Unexpectedly, a second phase of expression occurs at later stages of shark fin development, in which Hoxd12 and Hoxd13 are re-expressed along the distal margin of the fin buds. This second phase is similar to that observed in tetrapod limbs. The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans. We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.

Show MeSH
Related in: MedlinePlus