Limits...
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 Hoxd12 and Hoxd13 in the cloacal region of catsharks.(A) Lateral view of pelvic fin region showing Hoxd12 expression at stage 25. Dashed lines mark the approximate planes of section showed in panels B and C. (B) Transverse section showing Hoxd12 expression in visceral mesoderm (Vm) and gut endoderm (Ge). Note absence of Hoxd12 expression in anterior part of the pelvic fin (Pl). (C) Transverse section showing Hoxd12 expression in the posterior part of pelvic fin and adjacent visceral mesoderm. Note absence of Hoxd12 expression in the gut endoderm. (D) Lateral view of the pelvic fin region showing Hoxd13 expression at stage 25. Note that Hoxd13 domain lies posterior to Hoxd12 domain (compare with panel A). Dashed lines mark the approximate planes of the section showed in panels E and F. (E) Transverse section showing Hoxd13 expression in the visceral mesoderm and gut endoderm. Note absence of Hoxd13 expression in the anterior part of pelvic fin. (F) Transverse section showing Hoxd13 expression in the posterior part of the fin, visceral mesoderm and ventral endoderm. Arrowheads mark expression in endoderm (contrast with absence of Hoxd12 in endoderm in panel C). (G) Transverse section throughout the pelvic fins at stage 30 showing Hoxd13 expression in the cloacal epithelium (arrowheads).
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pone-0000754-g004: Expression of Hoxd12 and Hoxd13 in the cloacal region of catsharks.(A) Lateral view of pelvic fin region showing Hoxd12 expression at stage 25. Dashed lines mark the approximate planes of section showed in panels B and C. (B) Transverse section showing Hoxd12 expression in visceral mesoderm (Vm) and gut endoderm (Ge). Note absence of Hoxd12 expression in anterior part of the pelvic fin (Pl). (C) Transverse section showing Hoxd12 expression in the posterior part of pelvic fin and adjacent visceral mesoderm. Note absence of Hoxd12 expression in the gut endoderm. (D) Lateral view of the pelvic fin region showing Hoxd13 expression at stage 25. Note that Hoxd13 domain lies posterior to Hoxd12 domain (compare with panel A). Dashed lines mark the approximate planes of the section showed in panels E and F. (E) Transverse section showing Hoxd13 expression in the visceral mesoderm and gut endoderm. Note absence of Hoxd13 expression in the anterior part of pelvic fin. (F) Transverse section showing Hoxd13 expression in the posterior part of the fin, visceral mesoderm and ventral endoderm. Arrowheads mark expression in endoderm (contrast with absence of Hoxd12 in endoderm in panel C). (G) Transverse section throughout the pelvic fins at stage 30 showing Hoxd13 expression in the cloacal epithelium (arrowheads).

Mentions: Initiation of pelvic fin budding was preceded by the expression of Hoxd9 in the somatic layer of the lateral plate mesoderm at the cloacal level (Fig. 3A, stage 22). By the time pelvic fins emerged, however, Hoxd9 was no longer detectable in the fin mesenchyme (Fig. 3A, stage 25). Similarly, Hoxd10 was first expressed throughout the region of the prospective pelvic fins (Fig. 3B, stage 22), but by the onset of budding, Hoxd10 had become restricted to the posterior mesenchyme (Fig. 3B, stage 25). Hoxd12 was expressed in posterior mesenchyme of the pelvic fins from the initial stages of outgrowth (Fig. 3C and Fig. 4A–C). Hoxd13 was expressed even further posteriorly in pelvic appendages (Fig. 3D and Fig. 4D–F). Hoxd12 and Hoxd13 were maintained in the posterior regions of the pelvic fins, in the swellings from which the male claspers develop (Fig. 3C and 3D, stage 30). Both Hoxd12 and Hoxd13 then exhibited a second phase of expression, in domains that extended anteriorly as narrow bands of expression along the distal most mesenchyme of the pelvic fin buds (Fig. 3E, F). At stage 31, a new distal domain of Hoxd13 could be observed extending along the entire distal margin of the pelvic fin, and expression persisted throughout the distal-most mesenchyme at stage 32 (Fig. 3F). By stage 32, a narrow band of Hoxd12 expression also extended anterior to the clasper, immediately under the distal ectoderm (Fig. 3E). Thus, in the developing pectoral and pelvic fins of the catshark, 5′Hoxd genes are expressed in dynamic, biphasic patterns, and the second phase shows a reversal of temporal and spatial collinearity similar to that found in shark pectoral fins and in tetrapod limbs.


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 Hoxd12 and Hoxd13 in the cloacal region of catsharks.(A) Lateral view of pelvic fin region showing Hoxd12 expression at stage 25. Dashed lines mark the approximate planes of section showed in panels B and C. (B) Transverse section showing Hoxd12 expression in visceral mesoderm (Vm) and gut endoderm (Ge). Note absence of Hoxd12 expression in anterior part of the pelvic fin (Pl). (C) Transverse section showing Hoxd12 expression in the posterior part of pelvic fin and adjacent visceral mesoderm. Note absence of Hoxd12 expression in the gut endoderm. (D) Lateral view of the pelvic fin region showing Hoxd13 expression at stage 25. Note that Hoxd13 domain lies posterior to Hoxd12 domain (compare with panel A). Dashed lines mark the approximate planes of the section showed in panels E and F. (E) Transverse section showing Hoxd13 expression in the visceral mesoderm and gut endoderm. Note absence of Hoxd13 expression in the anterior part of pelvic fin. (F) Transverse section showing Hoxd13 expression in the posterior part of the fin, visceral mesoderm and ventral endoderm. Arrowheads mark expression in endoderm (contrast with absence of Hoxd12 in endoderm in panel C). (G) Transverse section throughout the pelvic fins at stage 30 showing Hoxd13 expression in the cloacal epithelium (arrowheads).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC1937022&req=5

pone-0000754-g004: Expression of Hoxd12 and Hoxd13 in the cloacal region of catsharks.(A) Lateral view of pelvic fin region showing Hoxd12 expression at stage 25. Dashed lines mark the approximate planes of section showed in panels B and C. (B) Transverse section showing Hoxd12 expression in visceral mesoderm (Vm) and gut endoderm (Ge). Note absence of Hoxd12 expression in anterior part of the pelvic fin (Pl). (C) Transverse section showing Hoxd12 expression in the posterior part of pelvic fin and adjacent visceral mesoderm. Note absence of Hoxd12 expression in the gut endoderm. (D) Lateral view of the pelvic fin region showing Hoxd13 expression at stage 25. Note that Hoxd13 domain lies posterior to Hoxd12 domain (compare with panel A). Dashed lines mark the approximate planes of the section showed in panels E and F. (E) Transverse section showing Hoxd13 expression in the visceral mesoderm and gut endoderm. Note absence of Hoxd13 expression in the anterior part of pelvic fin. (F) Transverse section showing Hoxd13 expression in the posterior part of the fin, visceral mesoderm and ventral endoderm. Arrowheads mark expression in endoderm (contrast with absence of Hoxd12 in endoderm in panel C). (G) Transverse section throughout the pelvic fins at stage 30 showing Hoxd13 expression in the cloacal epithelium (arrowheads).
Mentions: Initiation of pelvic fin budding was preceded by the expression of Hoxd9 in the somatic layer of the lateral plate mesoderm at the cloacal level (Fig. 3A, stage 22). By the time pelvic fins emerged, however, Hoxd9 was no longer detectable in the fin mesenchyme (Fig. 3A, stage 25). Similarly, Hoxd10 was first expressed throughout the region of the prospective pelvic fins (Fig. 3B, stage 22), but by the onset of budding, Hoxd10 had become restricted to the posterior mesenchyme (Fig. 3B, stage 25). Hoxd12 was expressed in posterior mesenchyme of the pelvic fins from the initial stages of outgrowth (Fig. 3C and Fig. 4A–C). Hoxd13 was expressed even further posteriorly in pelvic appendages (Fig. 3D and Fig. 4D–F). Hoxd12 and Hoxd13 were maintained in the posterior regions of the pelvic fins, in the swellings from which the male claspers develop (Fig. 3C and 3D, stage 30). Both Hoxd12 and Hoxd13 then exhibited a second phase of expression, in domains that extended anteriorly as narrow bands of expression along the distal most mesenchyme of the pelvic fin buds (Fig. 3E, F). At stage 31, a new distal domain of Hoxd13 could be observed extending along the entire distal margin of the pelvic fin, and expression persisted throughout the distal-most mesenchyme at stage 32 (Fig. 3F). By stage 32, a narrow band of Hoxd12 expression also extended anterior to the clasper, immediately under the distal ectoderm (Fig. 3E). Thus, in the developing pectoral and pelvic fins of the catshark, 5′Hoxd genes are expressed in dynamic, biphasic patterns, and the second phase shows a reversal of temporal and spatial collinearity similar to that found in shark pectoral fins and in tetrapod limbs.

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